Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants
Parasites are generally overdispersed among their hosts, with far-reaching implications for their population dynamics and control. The factors determining parasite overdispersion have long been debated. In particular, stochastic parasite acquisition and individual host variation in density-dependent...
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MDPI AG
2023-06-01
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| Series: | Animals |
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| Online Access: | https://www.mdpi.com/2076-2615/13/11/1882 |
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| author | Eric R. Morgan Anne Segonds-Pichon Hubert Ferté Patrick Duncan Jacques Cabaret |
| author_facet | Eric R. Morgan Anne Segonds-Pichon Hubert Ferté Patrick Duncan Jacques Cabaret |
| author_sort | Eric R. Morgan |
| collection | DOAJ |
| description | Parasites are generally overdispersed among their hosts, with far-reaching implications for their population dynamics and control. The factors determining parasite overdispersion have long been debated. In particular, stochastic parasite acquisition and individual host variation in density-dependent regulation through acquired host immunity have been identified as key factors, but their relative roles and possible interactions have seen little empirical exploration in parasite populations. Here, Taylor’s power law is applied to test the hypothesis that periodic parasite removal destabilises the host-parasite relationship and increases variance in parasite burden around the mean. The slope of the power relationship was compared by analysis of covariance among 325 nematode populations in wild and domestic ruminants, exploiting that domestic ruminants are often routinely treated against parasite infections. In <i>Haemonchus</i> spp. and <i>Trichostrongylus axei</i> in domestic livestock, the slope increased with the frequency of anthelmintic treatment, supporting this hypothesis. In <i>Nematodirus</i> spp., against which acquired immunity is known to be strong, the slope was significantly greater in post-mortem worm burden data than in faecal egg counts, while this relationship did not hold for the less immunogenic genus <i>Marshallagia</i>. Considered together, these findings suggest that immunity acting through an exposure-dependent reduction in parasite fecundity stabilises variance in faecal egg counts, reducing overdispersion, and that periodic anthelmintic treatment interferes with this process and increases overdispersion. The results have implications for the diagnosis and control of parasitic infections in domestic animals, which are complicated by overdispersion, and for our understanding of parasite distribution in free-living wildlife. Parasite-host systems, in which treatment and immunity effectively mimic metapopulation processes of patch extinction and density dependence, could also yield general insights into the spatio-temporal stability of animal distributions. |
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| issn | 2076-2615 |
| language | English |
| last_indexed | 2024-03-11T03:12:22Z |
| publishDate | 2023-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Animals |
| spelling | doaj.art-5350fbe7c11441528d775ef677b8585f2023-11-18T07:30:57ZengMDPI AGAnimals2076-26152023-06-011311188210.3390/ani13111882Anthelmintic Treatment and the Stability of Parasite Distribution in RuminantsEric R. Morgan0Anne Segonds-Pichon1Hubert Ferté2Patrick Duncan3Jacques Cabaret4School of Biological Sciences, Queen’s University Belfast, 19, Chlorine Gardens, Belfast BT9 5DL, UKBabraham Institute, Cambridge CB22 3AT, UKFaculté de Pharmacie, Université de Reims Champagne-Ardenne, SFR Cap Santé, EA7510 ESCAPE–USC VECPAR, 51 rue Cognacq-Jay, 51096 Reims, FranceCentre d’Etudes Biologiques de Chize, CNRS UPR 1934, 79360 Beauvoir-sur-Niort, FranceISP, INRAE, Université Tours, UMR1282, 37380 Nouzilly, FranceParasites are generally overdispersed among their hosts, with far-reaching implications for their population dynamics and control. The factors determining parasite overdispersion have long been debated. In particular, stochastic parasite acquisition and individual host variation in density-dependent regulation through acquired host immunity have been identified as key factors, but their relative roles and possible interactions have seen little empirical exploration in parasite populations. Here, Taylor’s power law is applied to test the hypothesis that periodic parasite removal destabilises the host-parasite relationship and increases variance in parasite burden around the mean. The slope of the power relationship was compared by analysis of covariance among 325 nematode populations in wild and domestic ruminants, exploiting that domestic ruminants are often routinely treated against parasite infections. In <i>Haemonchus</i> spp. and <i>Trichostrongylus axei</i> in domestic livestock, the slope increased with the frequency of anthelmintic treatment, supporting this hypothesis. In <i>Nematodirus</i> spp., against which acquired immunity is known to be strong, the slope was significantly greater in post-mortem worm burden data than in faecal egg counts, while this relationship did not hold for the less immunogenic genus <i>Marshallagia</i>. Considered together, these findings suggest that immunity acting through an exposure-dependent reduction in parasite fecundity stabilises variance in faecal egg counts, reducing overdispersion, and that periodic anthelmintic treatment interferes with this process and increases overdispersion. The results have implications for the diagnosis and control of parasitic infections in domestic animals, which are complicated by overdispersion, and for our understanding of parasite distribution in free-living wildlife. Parasite-host systems, in which treatment and immunity effectively mimic metapopulation processes of patch extinction and density dependence, could also yield general insights into the spatio-temporal stability of animal distributions.https://www.mdpi.com/2076-2615/13/11/1882parasiteaggregationoverdispersionmechanismTaylor’s power lawmetapopulation dynamics |
| spellingShingle | Eric R. Morgan Anne Segonds-Pichon Hubert Ferté Patrick Duncan Jacques Cabaret Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants Animals parasite aggregation overdispersion mechanism Taylor’s power law metapopulation dynamics |
| title | Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants |
| title_full | Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants |
| title_fullStr | Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants |
| title_full_unstemmed | Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants |
| title_short | Anthelmintic Treatment and the Stability of Parasite Distribution in Ruminants |
| title_sort | anthelmintic treatment and the stability of parasite distribution in ruminants |
| topic | parasite aggregation overdispersion mechanism Taylor’s power law metapopulation dynamics |
| url | https://www.mdpi.com/2076-2615/13/11/1882 |
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