Refugia or reservoir? Feral goats and their role in the maintenance and circulation of benzimidazole-resistant gastrointestinal nematodes on shared pastures

Abstract

Gastrointestinal nematodes threaten the productivity of grazing livestock and anthelmintic resistance has emerged globally. It is broadly understood that wild ruminants living in sympatry with livestock act as a positive source of refugia for anthelmintic-susceptible nematodes. However, they might also act as reservoirs of anthelmintic-resistant nematodes, contributing to the spread of anthelmintic resistance at a regional scale. Here, we sampled managed sheep and cattle together with feral goats within the same property in New South Wales, Australia. Internal transcribed spacer 2 (ITS-2) nemabiome metabarcoding identified 12 gastrointestinal nematodes (Cooperia oncophora, Cooperia punctata, Haemonchus contortus, Haemonchus placei, Nematodirus spathiger, Ostertagia ostertagi, Teladorsagia circumcincta, Oesophagostomum radiatum, Oesophagostomum venulosum, Trichostrongylus axei, Trichostrongylus colubriformis and Trichostrongylus rugatus). Isotype-1 β-tubulin metabarcoding targeting benzimidazole resistance polymorphisms identified 6 of these nematode species (C. oncophora, C. punctata, H. contortus, H. placei, O. ostertagi and T. circumcincta), with the remaining 3 genera unable to be identified to the species level (Nematodirus, Oesophagostomum, Trichostrongylus). Both ITS-2 and β-tubulin metabarcoding showed the presence of a cryptic species of T. circumcincta, known from domestic goats in France. Of the gastrointestinal nematodes detected via β-tubulin metabarcoding, H. contortus, T. circumcincta, Nematodirus and Trichostrongylus exhibited the presence of at least one resistance genotype. We found that generalist gastrointestinal nematodes in untreated feral goats had a similarly high frequency of the benzimidazole-resistant F200Y polymorphism as those nematodes in sheep and cattle. This suggests cross-transmission and maintenance of the resistant genotype within the wild ruminant population, affirming that wild ruminants should be considered potential reservoirs of anthelmintic resistance.

Cross-transmission of resistant gastrointestinal nematodes between wildlife and transhumant sheep

“…Besides the commonly found polymorphisms at codons 167 and 200 (Avramenko et al, 2019; Redman et al, 2015), we detected several mutations at codon 198, occurring in particular with high frequency on the sheep farm in Montagne de l’Oule. In contrast to our study, previous research had found polymorphisms at codon 198, but they were rare (Francis and Šlapeta, 2023; Ramünke et al, 2016).…”

“…For instance, benzimidazole-resistant nematodes have been detected in free-living populations of roe deer, Capreolus capreolus , living in sympatry with livestock (Chintoan-Uta et al, 2014; Nagy et al, 2017). To date, the role of wild ungulates in the epidemiology of resistant nematodes remains to be determined, but it has been suggested that wildlife may act as a reservoir of resistant nematodes for livestock (Brown et al, 2022; Chintoan-Uta et al, 2014; Francis and Šlapeta, 2023; Laca Megyesi et al, 2019; Walker and Morgan, 2014). However, to accurately evaluate the potential role of wildlife as reservoirs for anthelmintic resistant gastrointestinal nematodes, we need to investigate the presence of resistant nematodes in co-grazing wild and domestic ungulates in different contexts, (i.e., different host species, different landscapes, and under different climatic conditions).…”

Morphometric characteristics of the nematode Oesophagostomum venulosum (Nematoda, Strongylida) isolated from the domestic goat

“…venulosum, O. radiatum, O. columbianum, are among the most widespread gastrointestinal strongylids in domestic and wild small ruminants (Horak & Louw, 1977;Tariq et al, 2010;Mehlhorn, 2016;Halvarsson et al, 2022). Oesophagostomum radiatum and O. venulosum have been found in domestic sheep and wild goats in Australia (Francis & Šlapeta, 2023). Nematodes of the species O. venulosum have been found in moose (Alces alces), red deer (Cervus elaphus) and roe deer (Capreolus capreolus) in the Belarusian Polissia (Shimalov & Shimalov, 2003).…”