Reproductive females and young mouflon (<i>Ovis gmelini musimon</i>×<i>Ovis</i>sp.) in poor body condition are the main spreaders of gastrointestinal parasites

Bourgoin, Gilles; Portanier, Elodie; Poirel, Marie-Thérèse; Itty, Christian; Duhayer, Jeanne; Benabed, Slimania; Cockenpot, Anne; Callait-Cardinal, Marie-Pierre; Garel, Mathieu

doi:10.1017/s0031182021000329

Cited by 14 publications

(10 citation statements)

References 86 publications

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“…There is probably a synergistic interaction among the body condition of roe deer, their immune response and the richness of parasites to which they have been exposed [ 11 ]. Individuals in lower body condition are more susceptible to parasite infection or/and high levels of parasitism are suspected to negatively impact body condition [ 19 ]. Such negative correlation between physiological performance and parasitic burden has previously been observed to be more pronounced in Chizé than in Trois Fontaines [ 76 ].…”

Section: Discussionmentioning

confidence: 99%

“…roe deer [ 13 ], African buffalo, Syncerus caffer [ 18 ], mouflon, Ovis gmelini musimon × Ovis sp. [ 19 ], feral sheep [ 3 ]), and is generally higher in males [ 20 ]. The higher susceptibility of males to infection has been ascribed to the immunosuppressive effects of sex steroid hormones in males [ 21 ], sexual size dimorphism [ 22 ] and also increased likelihood of pathogen exposure [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

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Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes

et al. 2021

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Background Gastrointestinal nematodes are ubiquitous for both domestic and wild ungulates and have varying consequences for health and fitness. They exist as complex communities of multiple co-infecting species, and we have a limited understanding of how these communities vary in different hosts, regions and circumstances or of how this affects their impacts. Methods We have undertaken ITS2 rDNA nemabiome metabarcoding with next-generation sequencing on populations of nematode larvae isolated from 149 fecal samples of roe deer of different sex and age classes in the two isolated populations of Chizé and Trois Fontaines in France not co-grazing with any domestic ungulate species. Results We identified 100 amplified sequence variants (ASVs) that were assigned to 14 gastrointestinal nematode taxa overall at either genus (29%) or species (71%) level. These taxa were dominated by parasites classically found in cervids—e.g. Ostertagia leptospicularis, Spiculopteragia spp. Higher parasite species diversity was present in the Trois Fontaines population than in the Chizé population including the presence of species more typically seen in domestic livestock (Haemonchus contortus, Bunostomum sp., Cooperia punctata, Teladorsagia circumcincta). No differences in parasite species diversity or community composition were seen in the samples collected from three zones of differing habitat quality within the Chizé study area. Young roe deer hosted the highest diversity of gastrointestinal nematodes, with more pronounced effects of age apparent in Trois Fontaines. The effect of host age differed between gastrointestinal nematode species, e.g. there was little effect on O. leptospicularis but a large effect on Trichostrongylus spp. No effect of host sex was detected in either site. Conclusions The presence of some livestock parasite species in the Trois Fontaines roe deer population was unexpected given the isolation of this population away from grazing domestic livestock since decades. Overall, our results illustrate the influence of host traits and the local environment on roe deer nemabiome and demonstrate the power of the nemabiome metabarcoding approach to elucidate the composition of gastrointestinal nematode communities in wildlife. Graphical Abstract

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes

et al. 2021

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“…There is probably a synergistic interaction between the body condition of roe deer, their immune response and the richness of parasites to which they have been exposed [14]. Individuals in lower body condition are more susceptible to parasite infection or/and high levels of parasitism is suspected to negatively impact body condition [70]. Such negative correlation between physiological performance and parasitic burden was observed to be more pronounced in Chizé than in Trois Fontaines [71].…”

Section: Effects Of Site Age and Sex Class On The Nemabiomementioning

confidence: 99%

ITS-2 rDNA Nemabiome Metabarcoding in two Isolated Populations of Wild Roe Deer (Capreolus Capreolus) Reveals Variation in Gastrointestinal Nematode Community Composition Between Regions and Among Age Classes

Beaumelle

Redman

Rijke

et al. 2021

Preprint

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BackgroundGastrointestinal nematodes are ubiquitous for both domestic and wild ungulates which have varying consequences to health and fitness. They exist as complex communities of multiple co-infecting species and we have a very limited understanding of how these communities vary in different hosts, regions and circumstances or on how this affects their impacts. MethodsWe have undertaken ITS-2 rDNA nemabiome metabarcoding on populations of nematode larvae isolated from fecal samples of roe deer of different sex and age classes in the two isolated populations of Chizé and Trois Fontaines in France not co-grazing with any domestic ungulate species. ResultsWe identified 100 Amplified Sequence Variants (ASVs) that assigned to 14 gastrointestinal nematode taxa overall either at genus (38%), or species (62%) level. These taxa were dominated by parasites classically found in cervids - e.g., Ostertagia leptospicularis, Spiculopteragia spp. Higher parasite species diversity was present in the Trois Fontaine than in the Chize populations including the presence of some species more typically seen in domestic livestock, (Haemonchus contortus, Bunostomum trigonocephalum, Cooperia punctata, Teladorsagia circumcincta). No differences in parasite species diversity or community composition was seen in the samples collected from three zones of differing habitat quality within the Chize region. Young roe deer hosted the highest diversity of gastrointestinal nematodes, with more pronounced effects of age apparent in Trois Fontaines. The effect of host age differed between gastrointestinal nematode species, e.g. there was little effect on Ostertagia leptospicularis but a high effect on Trichostrongylus spp. No effect of host sex was detected in either site. ConclusionsThe presence of some livestock parasite species in the Trois Fontaine roe deer popualtions was surprising given the isolation of this population away from grazing domestic livestock. However, it should be noted that a small group of sheep were resident in the region, albeit separately fenced, which raises some interesting questions regarding the introduction of non-native parasite species into wildlife populations. Overall, our results suggest complex interactions between hosts, environments and parasites and illustrate the power of the nemabiome metabarcoding approach to elucidate the composition of gastrointestinal nematode communities in wildlife.

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“…Finally, measures of parasite load are of particular interest for monitoring GIN infections, as they correlate with host body condition, fecundity, and survival in populations of wild ungulates [ 55 , 56 ]. Traditional egg and larval count methods from faecal samples provide a non-invasive method for estimating parasite load, but involve laborious isolation procedures that make the method suboptimal for large-scale monitoring programs where high throughput of many samples is required.…”

Section: Discussionmentioning

confidence: 99%

Faecal metabarcoding provides improved detection and taxonomic resolution for non-invasive monitoring of gastrointestinal nematode parasites in wild moose populations

et al. 2023

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Background Although wild ungulate populations are heavily monitored throughout Europe, we understand little of how parasites affect population dynamics, and there is no systematic, long-term monitoring of parasite diversity and parasite loads. Such monitoring is in part hampered by a lack of time- and cost-effective assay methodologies with high sensitivity and good taxonomic resolution. DNA metabarcoding has been successfully used to characterize the parasitic nemabiome with high taxonomic resolution in a variety of wild and domestic hosts. However, in order to implement this technique in large-scale, potentially non-invasive monitoring of gastrointestinal parasitic nematodes (GIN), protocol optimization is required to maximize biodiversity detection, whilst maintaining time- and cost-effectiveness. Methods Faecal samples were collected from a wild moose population and GIN communities were characterized and quantified using both parasitological techniques (egg and larva counting) and DNA metabarcoding of the ITS2 region of rDNA. Three different isolation methods were compared that differed in the volume of starting material and cell lysis method. Results Similar nematode faunas were recovered from all samples using both parasitological and metabarcoding methods, and the approaches were largely congruent. However, metabarcoding assays showed better taxonomic resolution and slightly higher sensitivity than egg and larvae counts. The metabarcoding was not strictly quantitative, but the proportion of target nematode sequences recovered was correlated with the parasitologically determined parasite load. Species detection rates in the metabarcoding assays were maximized using a DNA isolation method that included mechanical cell disruption and maximized the starting material volume. Conclusions DNA metabarcoding is a promising technique for the non-invasive, large-scale monitoring of parasitic GINs in wild ungulate populations, owing to its high taxonomic resolution, increased assay sensitivity, and time- and cost-effectiveness. Although metabarcoding is not a strictly quantitative method, it may nonetheless be possible to create a management- and conservation-relevant index for the host parasite load from this data. To optimize the detection rates and time- and cost-effectiveness of metabarcoding assays, we recommend choosing a DNA isolation method that involves mechanical cell disruption and maximizes the starting material volume. Graphical Abstract

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Reproductive females and young mouflon (Ovis gmelini musimon×Ovissp.) in poor body condition are the main spreaders of gastrointestinal parasites

Abstract: Abstract

Cited by 14 publications

References 86 publications

Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes

Metabarcoding in two isolated populations of wild roe deer (Capreolus capreolus) reveals variation in gastrointestinal nematode community composition between regions and among age classes

ITS-2 rDNA Nemabiome Metabarcoding in two Isolated Populations of Wild Roe Deer (Capreolus Capreolus) Reveals Variation in Gastrointestinal Nematode Community Composition Between Regions and Among Age Classes

Faecal metabarcoding provides improved detection and taxonomic resolution for non-invasive monitoring of gastrointestinal nematode parasites in wild moose populations

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