High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding

Abstract Background The ability of infective larvae of cattle gastrointestinal nematode (GIN) species to overwinter on pastures in northerly climatic zones with very cold dry winters is poorly understood. This is an important knowledge gap with critical implications for parasite risk assessment and...

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Main Authors: Tong Wang, Russell W. Avramenko, Elizabeth M. Redman, Janneke Wit, John S. Gilleard, Douglas D. Colwell
Format: Article
Language:English
Published: BMC 2020-09-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-020-04337-2
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spelling doaj-b6afa1ecfc43434aa36e7c432b1a57a72020-11-25T03:33:31ZengBMCParasites & Vectors1756-33052020-09-0113111110.1186/s13071-020-04337-2High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcodingTong Wang0Russell W. Avramenko1Elizabeth M. Redman2Janneke Wit3John S. Gilleard4Douglas D. Colwell5Department of Comparative Biology and Experimental Medicine, Host-Parasite Interactions Program, Faculty of Veterinary Medicine, University of CalgaryDepartment of Comparative Biology and Experimental Medicine, Host-Parasite Interactions Program, Faculty of Veterinary Medicine, University of CalgaryDepartment of Comparative Biology and Experimental Medicine, Host-Parasite Interactions Program, Faculty of Veterinary Medicine, University of CalgaryDepartment of Comparative Biology and Experimental Medicine, Host-Parasite Interactions Program, Faculty of Veterinary Medicine, University of CalgaryDepartment of Comparative Biology and Experimental Medicine, Host-Parasite Interactions Program, Faculty of Veterinary Medicine, University of CalgaryLiverstock Parasitology, Agriculture and Agri-Food CanadaAbstract Background The ability of infective larvae of cattle gastrointestinal nematode (GIN) species to overwinter on pastures in northerly climatic zones with very cold dry winters is poorly understood. This is an important knowledge gap with critical implications for parasite risk assessment and control. Methods Infective third-stage larvae (L3) were quantified in samples of fecal pats, together with adjacent grass and soil, before and after winter on three farms in southern, central and northern Alberta. Nemabiome ITS2 metabarcoding was then performed on the harvested L3 populations to determine the species composition. Finally, parasite-free tracer calves were used to investigate if the L3 surviving the winter could infect calves and develop to adult worms in spring. Results Farm level monitoring, using solar powered weather stations, revealed that ground temperatures were consistently higher, and less variable, than the air temperatures; minimum winter air and ground temperatures were − 32.5 °C and − 24.7 °C respectively. In spite of the extremely low minimum temperatures reached, L3 were recovered from fecal pats and grass before and after winter with only a 38% and 61% overall reduction over the winter, respectively. Nemabiome ITS2 metabarcoding assay revealed that the proportion of L3 surviving the winter was high for both Cooperia oncophora and Ostertagia ostertagi although survival of the former species was statistically significantly higher than the latter. Nematodirus helvetinaus and Trichostrongylus axei could be detected after winter whereas Haemonchus placei L3 could not overwinter at all. Adult C. oncophora, O. ostertagi and N. helvetianus could be recovered from tracer calves grazing after the winter. Conclusions The largest proportion of L3 were recovered from fecal pats suggesting this is important refuge for L3 survival. Results also show that L3 of several GIN parasite species can survive relatively efficiently on pastures even in the extreme winter conditions in western Canada. Tracer calf experiments confirmed that overwintered L3 of both C. oncophora and O. ostertagi were capable of establishing a patent infection in the following spring. These results have important implications for the epidemiology, risk of production impact and the design of effective control strategies. The work also illustrates the value of applying ITS2 nemabiome metabarcoding to environmental samples.http://link.springer.com/article/10.1186/s13071-020-04337-2Gastrointestinal nematodesOverwinteringWestern CanadaITS2 rDNA metabarcodingTracer calves
collection DOAJ
language English
format Article
sources DOAJ
author Tong Wang
Russell W. Avramenko
Elizabeth M. Redman
Janneke Wit
John S. Gilleard
Douglas D. Colwell
spellingShingle Tong Wang
Russell W. Avramenko
Elizabeth M. Redman
Janneke Wit
John S. Gilleard
Douglas D. Colwell
High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding
Parasites & Vectors
Gastrointestinal nematodes
Overwintering
Western Canada
ITS2 rDNA metabarcoding
Tracer calves
author_facet Tong Wang
Russell W. Avramenko
Elizabeth M. Redman
Janneke Wit
John S. Gilleard
Douglas D. Colwell
author_sort Tong Wang
title High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding
title_short High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding
title_full High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding
title_fullStr High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding
title_full_unstemmed High levels of third-stage larvae (L3) overwinter survival for multiple cattle gastrointestinal nematode species on western Canadian pastures as revealed by ITS2 rDNA metabarcoding
title_sort high levels of third-stage larvae (l3) overwinter survival for multiple cattle gastrointestinal nematode species on western canadian pastures as revealed by its2 rdna metabarcoding
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2020-09-01
description Abstract Background The ability of infective larvae of cattle gastrointestinal nematode (GIN) species to overwinter on pastures in northerly climatic zones with very cold dry winters is poorly understood. This is an important knowledge gap with critical implications for parasite risk assessment and control. Methods Infective third-stage larvae (L3) were quantified in samples of fecal pats, together with adjacent grass and soil, before and after winter on three farms in southern, central and northern Alberta. Nemabiome ITS2 metabarcoding was then performed on the harvested L3 populations to determine the species composition. Finally, parasite-free tracer calves were used to investigate if the L3 surviving the winter could infect calves and develop to adult worms in spring. Results Farm level monitoring, using solar powered weather stations, revealed that ground temperatures were consistently higher, and less variable, than the air temperatures; minimum winter air and ground temperatures were − 32.5 °C and − 24.7 °C respectively. In spite of the extremely low minimum temperatures reached, L3 were recovered from fecal pats and grass before and after winter with only a 38% and 61% overall reduction over the winter, respectively. Nemabiome ITS2 metabarcoding assay revealed that the proportion of L3 surviving the winter was high for both Cooperia oncophora and Ostertagia ostertagi although survival of the former species was statistically significantly higher than the latter. Nematodirus helvetinaus and Trichostrongylus axei could be detected after winter whereas Haemonchus placei L3 could not overwinter at all. Adult C. oncophora, O. ostertagi and N. helvetianus could be recovered from tracer calves grazing after the winter. Conclusions The largest proportion of L3 were recovered from fecal pats suggesting this is important refuge for L3 survival. Results also show that L3 of several GIN parasite species can survive relatively efficiently on pastures even in the extreme winter conditions in western Canada. Tracer calf experiments confirmed that overwintered L3 of both C. oncophora and O. ostertagi were capable of establishing a patent infection in the following spring. These results have important implications for the epidemiology, risk of production impact and the design of effective control strategies. The work also illustrates the value of applying ITS2 nemabiome metabarcoding to environmental samples.
topic Gastrointestinal nematodes
Overwintering
Western Canada
ITS2 rDNA metabarcoding
Tracer calves
url http://link.springer.com/article/10.1186/s13071-020-04337-2
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