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Soil fungi enable the control of gastrointestinal nematodes in wild bovidae captive in a zoological park: a 4-year trial

Published online by Cambridge University Press:  04 March 2020

A. M. Palomero
Affiliation:
COPAR Research Group, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain
C. F. Cazapal-Monteiro
Affiliation:
COPAR Research Group, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain
E. Valderrábano
Affiliation:
Marcelle Natureza Zoological Park, Outeiro de Rei, Lugo, Spain
A. Paz-Silva
Affiliation:
COPAR Research Group, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain
R. Sánchez-Andrade
Affiliation:
COPAR Research Group, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain
M. S. Arias*
Affiliation:
COPAR Research Group, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain
*
Author for correspondence: M. S. Arias, E-mail: [email protected]

Abstract

The control of gastrointestinal nematodes among ruminants maintained in zoological parks remains difficult due to infective stages develop in the soil. For the purpose to improve the possibilities of the control of gastrointestinal nematodes (genera Trichostrongylus, Nematodirus, Chabertia and Haemonchus) affecting wild captive bovidae ruminants belonging to the subfamilies Antilopinae, Caprinae, Bovinae and Reduncinae, commercial pelleted feed enriched with a blend of 104–105 spores of both filamentous fungi Mucor circinelloides + Duddingtonia flagrans per kg meal was provided for a period of 3.5 years. All animals were dewormed at the beginning of the trial and also when exceeding a cut-off point of 300 eggs per gram of feces (EPG). The anthelmintic efficacy ranged between 96 and 100%. The need for repeating the administration of parasiticide treatment disappeared at the 24th month of study in the Antilopinae individuals, and at the 8th month in the Caprinae, Bovinae and Reduncinae. No side-effects were observed on the skin or in the digestive, respiratory or reproductive system. It was concluded that this strategy provides a sustainable tool for preventing the contamination of paddocks where captive ruminants are maintained, decreasing the risk of infection by gastrointestinal nematodes and consequently the need of frequent deworming.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abaigar, T, Ortiz, J, Cano, M, Martinez-Carrasco, C, Albaladejo, A and Alonso, FD (1995) Effect of mebendazole and ivermectin on the shedding of nematode eggs by three species of gazelles (Gazella dama mhorr, G. cuvieri, and G. dorcas). Journal of Zoo and Wildlife Medicine 26, 392395.Google Scholar
Arias, MS, Cazapal-Monteiro, CF, Valderrábano, E, Miguélez, S, Rois, JL, López-Arellano, ME, Madeira de Carvalho, LM and de Gives, M (2013) A preliminary study of the biological control of strongyles affecting equids in a zoological park. Journal of Equine Veterinary Science 33, 11151120.Google Scholar
Arroyo, F, Hernández, JA, Cazapal-Monteiro, CF, Pedreira, J, Sanchís, J, Romasanta, Á, Sánchez-Andrade, R, Paz-Silva, A and Arias, MS (2017) Effect of the filamentous fungus Mucor circinelloides on the development of eggs of the rumen fluke Calicophoron daubneyi (Paramphistomidae). Journal of Parasitology 103, 199206.CrossRefGoogle Scholar
Braga, FR, Carvalho, RO, Araujo, JM, Silva, AR, Araújo, JV, Lima, WS, Tavela, AO and Ferreira, SR (2009) Predatory activity of the fungi Duddingtonia flagrans, Monacrosporium thaumasium, Monacrosporium sinense and Arthrobotrys robusta on Angiostrongylus vasorum first-stage larvae. Journal of Helminthology 83, 303308.CrossRefGoogle ScholarPubMed
Campos, AK, Araújo, JV, Guimarães, MP and Dias, AS (2009) Resistance of different fungal structures of Duddingtonia flagrans to the digestive process and predatory ability on larvae of Haemonchus contortus and Strongyloides papillosus in goat feces. Parasitology Research 105, 913919.CrossRefGoogle ScholarPubMed
Citino, SB (2003) Bovidae (except sheep and goat) and antilocapridae. In Fowler, ME and Miller, RE (eds), Zoo & Wild Animal Medicine, 5th Edn. Philadelphia, USA: Saunders WB, p. 672.Google Scholar
Daniels, SP and Proudman, CJ (2016) Ovicidal efficacy of fenbendazole after treatment of horses naturally infected with cyathostomins. Veterinary Parasitology 227, 151156.CrossRefGoogle ScholarPubMed
Fagiolini, M, Lia, RP, Laricchiuta, P, Cavicchio, P, Mannella, R, Cafarchia, C, Otranto, D, Finotello, R and Perrucci, S (2010) Gastrointestinal parasites in mammals of two Italian zoological gardens. Journal of Zoo Wildlife Medicine 41, 662670.CrossRefGoogle ScholarPubMed
Flack, S (2016) The Art and Science of Grazing: How Grass Farmers can Create Sustainable Systems for Healthy Animals and Farm Ecosystems. Vermont, VT, USA: Chelsea Green Publishing.Google Scholar
Goossens, E, Dorny, P, Boomker, J, Vercammen, F and Vercruysse, J (2005) A 12-month survey of the gastro-intestinal helminths of antelopes, gazelles and giraffids kept at two zoos in Belgium. Veterinary Parasitology 127, 303312.CrossRefGoogle ScholarPubMed
Hernández, , Arroyo, FL, Suárez, J, Cazapal-Monteiro, CF, Romasanta, Á, López-Arellano, ME, Pedreira, J, de Carvalho, LMM, Sánchez-Andrade, R, Arias, MS, de Gives, PM and Paz-Silva, A (2016) Feeding horses with industrially manufactured pellets with fungal spores to promote nematode integrated control. Veterinary Parasitology 229, 3744.CrossRefGoogle ScholarPubMed
Hernández, , Sánchez-Andrade, R, Cazapal-Monteiro, CF, Sanchís, JM, Arroyo, FL, Paz-Silva, A and Arias, MS (2018a) A combined effort to avoid strongyle infection in horses in an oceanic climate region: rotational grazing and parasiticidal fungi. Parasite & Vectors 11, 240247.CrossRefGoogle Scholar
Hernández, , Cazapal-Monteiro, CF, Sanchís, J, Sánchez-Andrade, R, Paz-Silva, A and Arias, MS (2018b) Potential usefulness of filamentous fungi to prevent zoonotic soil-transmitted helminths. Vector-Borne and Zoonotic Diseases 18, 690696.CrossRefGoogle Scholar
Hernández, , Cazapal-Monteiro, CF, Arroyo, FL, Silva, MI, Palomero, AM, Paz-Silva, A, Sánchez-Andrade, R and Arias, MS (2018c) Biological control of soil transmitted helminths (STHs) in a zoological park by using saprophytic fungi. Biological Control 122, 2430.CrossRefGoogle Scholar
Hiura, E, Del Carmen Garcia Lopes, A, da Paz, JS, Gava, MG, Flecher, MC, Colares, M, de Freitas Soares, FE, da Fonseca, LA, Lacerda, T, de Araújo, JV and Braga, FR (2015) Fungi predatory activity on embryonated Toxocara canis eggs inoculated in domestic chickens (Gallus gallus domesticus) and destruction of second stage larvae. Parasitology Research 114, 33013308.CrossRefGoogle ScholarPubMed
Maesano, G, Capasso, M, Ianniello, D, Cringoli, G and Rinaldi, L (2014) Parasitic infections detected by FLOTAC in zoo mammals from Warsaw, Poland. Acta Parasitologica 59, 343353.CrossRefGoogle ScholarPubMed
Mendoza-de Gives, P, López-Arellano, ME, Aguilar-Marcelino, L, Olazarán-Jenkins, S, Reyes-Guerrero, D, Ramírez-Várgas, G and Vega-Murillo, VE (2018) The nematophagous fungus Duddingtonia flagrans reduces the gastrointestinal parasitic nematode larvae population in faeces of orally treated calves maintained under tropical conditions-dose/response assessment. Veterinary Parasitology 263, 6672.CrossRefGoogle ScholarPubMed
Nosal, P, Kowal, J, Kornaś, S, Wyrobisz, A, Skotnicki, J, Basiaga, M and Plucińska, NE (2016) Endoparasites of exotic ungulates from the Giraffidae and Camelidae families kept ex situ. Annals of Parasitology 62, 6770.Google ScholarPubMed
Ortiz, J, De Ybañez MR, R, Abaigar, T, Goyena, M, Espeso, G, Cano, M and Alonso, F (2001) Effect of different methods of administration of ivermectin on its efficacy against the shedding of gastrointestinal nematode eggs by gazelles. Veterinary Record 149, 1215.CrossRefGoogle ScholarPubMed
Palomero, AM, Hernández, JA, Cazapal-Monteiro, CF, Balán, FA, Silva, MI, Paz-Silva, A, Sánchez-Andrade, R and Vázquez, MSA (2018) Implementation of biological control to the integrated control of strongyle infection among wild captive equids in a zoological park. BioMed Research International 2018, 4267683. doi: 10.1155/2018/4267683CrossRefGoogle Scholar
Panayotova-Pencheva, MS (2016) Experience in the ivermectin treatment of internal parasites in zoo and captive wild animals: a review. Der Zoologische Garten 85, 80308.CrossRefGoogle Scholar
Santos, MC, Silva, BF and Amarante, AF (2012) Environmental factors influencing the transmission of Haemonchus contortus. Veterinary Parasitology 188, 277284.CrossRefGoogle ScholarPubMed
Smith, M and Sherman, D (2009) Goat Medicine, 2nd Edn. Ames, IA, USA: Blackwell Publishing Ltd.Google Scholar
Thapa, S, Thamsborg, SM, Wang, R, Meyling, NV, Dalgaard, TS, Petersen, HH and Mejer, H (2018) Effect of the nematophagous fungus Pochonia chlamydosporia on soil content of ascarid eggs and infection levels in exposed hens. Parasites & Vectors 11, 319.CrossRefGoogle ScholarPubMed
Undersander, D, Albert, B, Cosgrove, D, Johnson, D and Peterson, P (2002) Pastures for Profit: A Guide to Rotational Grazing (A3529). Wisconsin, USA: Cooperative Extension Publishing, University of Wisconsin-Extension. Available at http://learningstore.uwex.edu/pdf/A3529.pdf.Google Scholar
Van Wyk, JA and Mayhew, E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Onderstepoort Journal of Veterinary Research 80, 539.CrossRefGoogle ScholarPubMed
Vieira, ÍS, Oliveira, IC, Campos, AK and Araújo, JV (2019) Association and predatory capacity of fungi Pochonia chlamydosporia and Arthrobotrys cladodes in the biological control of parasitic helminths of bovines. Parasitology 146, 13471351.CrossRefGoogle ScholarPubMed