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The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions

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A special issue of Journal of Zoological and Botanical Gardens (ISSN 2673-5636).

Deadline for manuscript submissions: closed (30 April 2024) | Viewed by 16438

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Dr. Mariana Panayotova-Pencheva

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Department of Experimental Parasitology, Institute of Experimental Morphology, Pathology and Anthropology with Museum, Bulgarian Academy of Sciences, Sofia, Bulgaria
Interests: veterinary parasitology; parasitic diseases; parasitic zoonoses; wildlife parasitoses

Special Issue Information

Dear Colleagues,

Parasitism is a widespread biological phenomenon in nature, and has also forever accompanied life in zoological gardens. The negative effects of parasitic infections in zoo animals could be numerous: the development of secondary deficiency and other infections, an impairment of reproduction, and a risk of death in cases of massive and dangerous parasitoses. Moreover, zoos are places where wild animals come into close contact with humans. This significantly increases the risk of the spread of parasitic zoonoses, posing a threat to the health of the animals themselves, staff of the zoos, and visitors.

The fight against parasitoses in zoos faces various challenges such as deficiencies in preventive programs; untimely or inaccurate diagnosis; parasite import via intermediates, paratenic hosts, or mechanical vectors (snails, ants, cockroaches, other insects, worms, rodents, etc.); persistent infections (e.g., soil-transmitted helminthoses); the need to adapt the antiparasitic treatment for a specific animal species, the development of resistance to drugs; and others. Success in this fight requires the united efforts of all zoo professionals: managers, curators, keepers, and veterinarians.

The help of science would be important but sometimes decisive for controlling parasitic diseases in zoo animals. The purpose of this Special Issue is to collect scientific papers on the topic of parasites in zoo animals that would contribute to both fundamental parasitology and zoo management practices. Original research articles, review articles, short communications, and case reports on all aspects of the subject are welcome. Let us do our part for a better future for animals in captivity!

Dr. Mariana Stancheva Panayotova-Pencheva
Guest Editor

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Keywords

parasite diversity in zoos
parasitological diagnostics
captive wildlife parasitoses
antiparasitic preventive programs in zoos
parasite treatment in wild animals
antiparasitic drugs for exotic animals
antiparasitic resistance

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Published Papers (9 papers)

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9 pages, 510 KiB

Open AccessArticle

Gastrointestinal Parasites in Reptiles from a Portuguese Zoo

by David Dantas, Cláudia Luís Batista, Maria João Castro, Nuno Alvura and Teresa Letra Mateus

J. Zool. Bot. Gard. 2025, 6(1), 12; https://doi.org/10.3390/jzbg6010012 - 7 Feb 2025

Viewed by 908

Abstract

The growing popularity of reptiles has contributed to their reproduction in captivity. When subjected to stressful environments, such as the presence of a higher number of humans and animals, reptiles may become more susceptible to parasites. Endoparasites in captive animals may cause several clinical signs ranging from mild to severe: lethargy, anorexia, diarrhea, cloacal/penile prolapse, infertility, intestinal malabsorption syndrome, and weight loss, among others. This study aimed to assess the presence of gastrointestinal parasites in fecal samples of reptiles from a Portuguese zoo through two techniques: a fecal flotation test (using a saturated sodium chloride solution) and Mini-FLOTAC. Ninety-nine samples belonging to 22 different animal species were collected and analyzed. Parasites were identified in 53.5% of the samples. Chelonians had a higher frequency (100%), followed by lizards (56.8%) and snakes (47.4%). The eggs/oocysts found were oxyurids (36.4%), strongylids/Kalicephalus sp. (8.1%), Eimeria sp. (5.1%), Hymenolepis spp. (5.1%), ascarids (4.0%), and Isospora sp. (2.0%). Both techniques presented the same results for each sample. The high prevalence of oxyurids, as well as of other parasites, can be explained by possible environmental contamination as these reptiles are kept in captivity. This study indicated the importance of assessing parasitic infections in reptiles in zoos, where routine coprological examinations should always be considered, as well as adequate prophylaxis. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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15 pages, 1951 KiB

Open AccessArticle

The Difficulties of Ex Situ Conservation: A Nationwide Investigation of Avian Haemosporidia Among Captive Penguins in Japan

by Mizue Inumaru, Misa Shimizu, Ayumi Shibata, Koichi Murata and Yukita Sato

J. Zool. Bot. Gard. 2025, 6(1), 7; https://doi.org/10.3390/jzbg6010007 - 1 Feb 2025

Viewed by 1188

Abstract

Avian malaria has been a continuous problem in both wild and captive populations of penguins throughout the world. In Japan, where there are over 3000 captive penguins, avian malaria (by Plasmodium spp.) and haemoproteosis (by Haemoproteus spp.) have been sporadically detected throughout the country. However, no comprehensive studies have been carried out, and the national status of infection has been unknown until now. In this study, the prevalence and lineage composition of haemosporidian parasites was investigated in captive penguins throughout Japan for the first time. A total of 1203 penguins from 55 facilities were sampled from January 2010 to December 2019. Parasites were detected by nested PCR and microscopy of blood and tissue samples. The total prevalence was 7.48% for Plasmodium and 1.75% for Haemoproteus, of which some are suggested to have been acquired during the study period. The odds of infection were higher in individuals kept outdoors compared to indoors, re-confirming that exposure to vectors is one of the major factors. Additionally, the odds of death were higher in infected individuals, although differences between parasite lineages were also observed. This study provides an overview of avian malaria in penguins of Japan in the hope of guiding future studies and conservation actions in captivity. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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11 pages, 3035 KiB

Open AccessArticle

A New Soil-Based Solution for Reducing the Persistence of Parasites in Zoos

by José Ángel Hernández, Cándido Viña, João Lozano, Izaro Zubiría, Miguel Baena, Inês Abreu-Ramos, Rami Salmo, Esther Valderrábano, Gustavo Pérez-Anzúrez, Adolfo Paz-Silva, Rodrigo Muíño, Cristiana Cazapal-Monteiro, María Sol Arias and Mercedes Camiña

J. Zool. Bot. Gard. 2024, 5(4), 817-827; https://doi.org/10.3390/jzbg5040054 - 20 Dec 2024

Viewed by 1006

Abstract

Controlling parasites in zoo animals is a significant challenge, making practical infection prevention methods essential. This study evaluated a novel solution using parasitophagous fungi-treated forage seeds to reduce soil parasite persistence. We conducted two experiments to assess the soil distribution of the fungi Mucor circinelloides (ovicidal) and Duddingtonia flagrans (larvicidal). Forage seeds were immersed in a submerged culture containing 10⁶ spores/mL and subsequently sown in plastic trays (trial 1) and demarcated ground plots (40 × 30 cm) framed with wood (trial 2). Fifteen days later, Ascaris suum and cyathostomin eggs were placed above the germinated vegetation. After a 25–30-day period, the viability of roundworm eggs reduced by 62%, and half of them remained undeveloped; a 64% reduction in the counts of L3 cyathostomins was recorded. In trial 2, viability decreased by 55% in roundworm eggs, with an infectivity rate of 30%, while L3 counts lessened by 57%. It has been concluded that the risk of infection by ascarids and cyathostomins can be reduced by at least half by sowing the soil with forage seeds pre-treated with fungi, providing a practical solution for parasite control in zoos. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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20 pages, 5239 KiB

Open AccessArticle

Parasitic Protozoa and Other Vector-Borne Pathogens in Captive Mammals from Brazil

by Anisleidy Pérez Castillo, Nicolas Colácio, Pedro Henrique Cotrin Rodrigues, João Victor Oliveira Miranda, Paula Cristina Senra Lima, Rafael Otávio Cançado Motta, Herlandes Penha Tinoco, Carlyle Mendes Coelho and Júlia Angélica Gonçalves da Silveira

J. Zool. Bot. Gard. 2024, 5(4), 754-773; https://doi.org/10.3390/jzbg5040050 - 2 Dec 2024

Cited by 1 | Viewed by 1493

Abstract

In captive environments, mammals are frequently exposed to various parasitic protozoa and other vector-borne pathogens that can impact both animal health and public health. Monitoring these pathogens is essential for animal welfare and zoonotic disease control. This study aimed to investigate the prevalence of parasitic protozoa and other vector-borne pathogens in captive mammals through molecular detection methods at the Belo Horizonte Zoo, Brazil. Between November 2021 and March 2023, whole blood samples were collected from 40 mammals. Molecular analyses identified piroplasms, Leishmania spp., granulocytic/platelet Anaplasma/Ehrlichia spp., monocytic Ehrlichia spp., Bartonella spp. and hemotropic Mycoplasma spp. with a 72.5% positivity rate. Piroplasms were found in 22.5% (two Pantanal cats, two gorillas, one white rhinoceros, one spider monkey, one jaguar, one tufted capuchin and one hippo) and Leishmania spp. in 12.9% (four maned wolves). Granulocytic/platelet Anaplasma/Ehrlichia spp. were found in 12.5% of the samples (one gorilla and four maned wolves), Ehrlichia canis in 2.5% of the animals (one maned wolf), Bartonella spp. in 42.5% (six howler monkeys, two maned wolves, one gorilla, one white rhino, one southern tamandua, one common woolly monkey, one tufted capuchin, one brown brocket deer, one agouti, one cougar and one hippo), hemotropic Mycoplasma spp. in 17.5% (one gorilla, one maned wolf, one white rhino, one howler monkey, two common woolly monkeys and one European fallow deer). Five Artiodactyla members tested negative for A. marginale. Coinfections occurred in 34.5% of the positive samples. Sequencing revealed that Theileria spp. and Cytauxzoon spp. are closely related to Theileria bicornis and Cytauxzoon felis; Ehrlichia canis and Bartonella spp. are closely related to B. clarridgeiae and B. henselae; and hemotropic Mycoplasma spp. are closely related to Candidatus Mycoplasma haemominutum. Our results showed a high occurrence of vector-borne pathogens in captive animals, including zoonotic species, which may pose a risk to animal and human public health. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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12 pages, 2259 KiB

Open AccessArticle

Gastrointestinal Parasitic Infections in Non-Human Primates at Gabon’s Primatology Center: Implications for Zoonotic Diseases

by Krista Mapagha-Boundoukou, Mohamed Hassani Mohamed-Djawad, Neil Michel Longo-Pendy, Patrice Makouloutou-Nzassi, Félicien Bangueboussa, Mourad Ben Said, Barthélémy Ngoubangoye and Larson Boundenga

J. Zool. Bot. Gard. 2024, 5(4), 733-744; https://doi.org/10.3390/jzbg5040048 - 19 Nov 2024

Viewed by 1671

Abstract

Parasites and infectious diseases pose significant threats to primate populations, especially in captive non-human primates (NHPs). This study aimed to assess the diversity and prevalence of intestinal parasites in NHPs at the CIRMF Primatology Center. A total of 97 fecal samples were analyzed using parasitological techniques, including sodium chloride flotation and modified Baermann sedimentation methods. An overall parasite prevalence of 93.81% (91/97) was observed. Sixteen groups of parasites with zoonotic potential were identified, comprising ten genera of nematodes (Trichuris, Enterobius, Hookworm, Trichostrongylus, Mammomonogamus, Spirure, Oesophagostomum, Schistosoma, Ascaris, and Strongyloides), three genera of protists (Eimeria, Balantioides coli/Buxtonella, and Entamoeba), one genus of cestodes (Hymenolepis), and two genera of trematodes (Dicrocoelium and Paramphistomum). High prevalences were noted for Oesophagostomum spp. (83.5%), Strongyloides spp. (52.58%), and Trichostrongylus spp. (50.52%). These findings underscore the potential role of the CIRMF Primatology Center in maintaining and facilitating the transmission of intestinal parasites with high zoonotic potential. The co-existence of human and NHP parasites in shared environments, such as zoos and research facilities, emphasizes the need for a holistic, One Health approach that addresses the interconnected health of humans, animals, and the environment. This study highlights the urgent need for collaborative strategies to mitigate the risks of zoonotic parasite transmission between NHPs and humans in captive settings. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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15 pages, 3796 KiB

Open AccessArticle

Coprological Survey of Helminths in Reindeer (Rangifer tarandus) in 50 Selected Zoos and Menageries in Russia

by Olga A. Loginova, Svetlana V. Akulova, Dmitry N. Egorov, Natalia S. Egorova, Sergei E. Spiridonov, Iuliia K. Plotnikova, Larisa M. Belova, Yuriy E. Kuznetsov, Daria I. Chuprak, Anna A. Krutikova, Iuliia V. Vasilkova, Diana A. Gelashvili, Yuri A. Shchepanovsky, Ivan A. Mizin, Danila V. Panchenko, Mikhail G. Bondar and Taras P. Sipko

J. Zool. Bot. Gard. 2024, 5(3), 492-506; https://doi.org/10.3390/jzbg5030033 - 12 Aug 2024

Viewed by 1535

Abstract

Zoo conditions are unique for reindeer, since domestic reindeer are not kept in captive facilities like cattle. In the zoo, reindeer are usually surrounded by many different animals that they would never encounter naturally. Thus, they might be infected with new helminths. Numerous petting zoos raise concerns about the safety of tactile interactions for human visitors. Our study is the first large-scale one. Qualitative and quantitative fecal analyses were carried out for 233 reindeer distributed over 50 Russian zoos according to the National Standard of the Russian Federation (GOST R 54627-2011) Ruminant animals—Methods of Laboratory Helminthological Diagnostics. Where possible, DNA analyses of helminths were performed targeting internal transcribed spacer region. As a result, F. hepatica, Paramphistomum sp., Moniezia sp. (including M. expansa), gastrointestinal strongylids (including Nematodirus spp.), Dictyocaulus sp., E. rangiferi, Trichuris sp., and Capillaria sp. were found in 106 (45%) zoo reindeer. All these helminths were previously reported in reindeer and pose no direct danger for humans. The intensity of invasions was mostly low. Fecal examination might be considered as an indirect method for mange diagnostics, as Chorioptes and Demodex mites were found in reindeer fecal samples. The latter may represent a novel species of mite specific for reindeer. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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11 pages, 2382 KiB

Open AccessArticle

Testing Mini-FLOTAC for the Monitorization of Gastrointestinal Parasitic Infections in Birds Kept at Four Iberian Zoological Institutions

by João Lozano, Cándido Pombo, Rami Salmo, Cristiana Cazapal-Monteiro, María Sol Arias, Daniela Carvalho, Madalena Lordelo, Augusto Batista, Rui Bernardino, Laura Rinaldi, Manuela Oliveira, Adolfo Paz-Silva and Luís Madeira de Carvalho

J. Zool. Bot. Gard. 2024, 5(2), 294-304; https://doi.org/10.3390/jzbg5020020 - 8 Jun 2024

Viewed by 1785

Abstract

Birds kept in zoological institutions are highly exposed to gastrointestinal (GI) parasitism caused by coccidia and nematodes. The current research aimed to characterize the avian GI parasitic fauna in several zoological collections in Portugal and Spain. During the full year of 2022, a total of 120 fecal samples were collected from four zoological institutions: Lisbon Zoo, Olivais Pedagogical Farm, and Avian Biodiversity Center (Lisbon, Portugal), and Avifauna park (Lugo, Spain). Analysis was conducted in domestic bird species (autochthonous and exotic poultry breeds), and 18 different exotic bird species like Galliformes (peacock, pheasant), Anseriformes (duck), Psittaciformes (parrot, macaw, cockatiel, parakeet, cockatoo), Coraciiformes (motmot), Charadriiformes (avocet), Strigiformes (owl), Phoenicopteriformes (flamingo), Struthioniformes (ostrich), Rheiformes (rhea), and Casuariiformes (emu, cassowary). Feces were processed using Mini-FLOTAC (MF), to identify parasitic forms and quantify their shedding (oocysts or eggs per gram of feces). Moreover, 15 fecal samples from pheasants were also processed using the McMaster method (McM), to compare the parasite shedding and frequencies between techniques. MF implementation allowed identification of coccidia infections in all bird collections. Also, peacocks of the Lisbon Zoo tested positive for Trichostrongylus tenuis and Strongyloides pavonis, and the exotic birds from Avifauna park were also positive for several nematode species, with Ascaridia sp., Capillaria sp., Strongyloides sp., and Syngamus trachea eggs being detected in pheasants’ feces. Moreover, the analysis of pheasants’ feces with MF detected prevalences of 33% for coccidia oocysts, and 47% for Capillaria sp. and Ascaridia sp. eggs, while McM detected prevalences of 13%, 27%, and 40% for the respective parasite taxa, with no differences being observed between methods (p = 0.39, p = 0.45, and p = 0.50, respectively). This research provided more scientific support regarding the importance of using Mini-FLOTAC in routine parasitological diagnosis in birds kept at zoological institutions. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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12 pages, 2770 KiB

Open AccessArticle

Respiratory Infection by Cyathostoma (Hovorkonema) americana in a Population of Burrowing Owls (Athene cunicularia)—A Potential Case of Zoo–Wildlife Cross-Transmission

by Gonçalo N. Marques, João T. Cruz, Matilde Pinto, Miriam Leal, Carla Flanagan, Nuno Urbani and Luís Madeira de Carvalho

J. Zool. Bot. Gard. 2023, 4(4), 788-799; https://doi.org/10.3390/jzbg4040056 - 5 Dec 2023

Viewed by 2579

Abstract

A population of burrowing owls (Athene cunicularia) under professional care at Zoomarine Portugal presented with sudden respiratory clinical signs. Clinical management included a thorough diagnosis plan, including in-house fecal analysis that revealed the presence of ovoid unioperculate eggs. In the postmortem examination of one hyperacute dyspneic specimen, adult nematode parasites were collected and identified based on their morphology as Cyathostoma (Hovorkonema) americana. Even after a broad-spectrum deworming protocol as part of the treatment and metaphylaxis approach, the incidence of parasitic reinfection was high. The complete clinical resolution was only accomplished after the identification and management of the possible focus of infection, a wild population of cattle egrets (Bubulcus ibis) that frequently congregated above the owls’ habitat. To the authors’ best knowledge, this is the first report of infection by Cyathostoma (Hovorkonema) americana in burrowing owls. Although nematodes of the family Syngamidae are not commonly included in the differential diagnosis of infectious respiratory agents of birds of the order Strigiformes, this report highlights the possibility of opportunistic parasitism in a zoological context, especially where there is a continued proximity to free-ranging avifauna. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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10 pages, 1919 KiB

Open AccessCase Report

Severe Parasite Co-Infection in a Captive Bactrian Camel: Case Report

by Mariana Panayotova-Pencheva and Francisco Ponce-Gordo

J. Zool. Bot. Gard. 2023, 4(4), 728-737; https://doi.org/10.3390/jzbg4040051 - 11 Nov 2023

Cited by 2 | Viewed by 2106

Abstract

The aim of this study was to document a case of parasite co-infection in a captive Bactrian camel and to supply morphometric data of the found pathogens. It concerned a 20-year-old male animal inhabiting Sofia Zoo, Bulgaria. A decreased appetite and gastrointestinal disorders were observed in it during the summer of 2022. Improvement in the animal’s condition was achieved after the administration of antibiotics, sulfonamides, and other symptomatic medicines. However, two weeks after treatment, clinical symptoms reappeared. Then, a diarrheal fecal sample from the animal was subjected to parasitological examination by direct smear and flotation and sedimentation techniques. Multiple infections by helminths (Trichostrongylus sp., Haemonchus sp., Oesophagostomum sp., Trichuris sp., and Dicrocoelium sp.), ciliates (Buxtonella cameli), and protozoa (Eimeria cameli) were found, with E. cameli being reported for the first time in zoo conditions. Deworming led to the recovery of the general condition and appearance of the animal’s feces, but two weeks later, it died suddenly. We considered that the parasitic infection was not the direct cause of the fatal outcome, and its presence, other health disorders, and the advanced age of the animal were among the contributing factors. This case reveals the need to combine planned preventive deworming with routine parasitological diagnostics to take timely and targeted actions to protect the health of animals inhabiting zoo facilities. Full article

(This article belongs to the Special Issue The Long-Standing Problem of Parasitic Diseases in Zoo Animals: Current Challenges and Searching for Solutions)

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