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Stability of within-host-parasite communities in a wild mammal system.

Knowles SC, Fenton A, Petchey OL, Jones TR, Barber R, Pedersen AB - Proc. Biol. Sci. (2013)

Bottom Line: Overall, these parasite communities were remarkably stable to perturbation.Only one non-target parasite species responded to deworming, and this response was temporary: we found strong, but short-lived, increases in the abundance of Eimeria protozoa, which share an infection site with the dominant nematode species, suggesting local, dynamic competition.These results, providing a rare and clear experimental demonstration of interactions between helminths and co-infecting parasites in wild vertebrates, constitute an important step towards understanding the wider consequences of similar drug treatments in humans and animals.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Biology, and Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK. s.knowles@imperial.ac.uk

ABSTRACT
Simultaneous infection by multiple parasite species is ubiquitous in nature. Interactions among co-infecting parasites may have important consequences for disease severity, transmission and community-level responses to perturbations. However, our current view of parasite interactions in nature comes primarily from observational studies, which may be unreliable at detecting interactions. We performed a perturbation experiment in wild mice, by using an anthelminthic to suppress nematodes, and monitored the consequences for other parasite species. Overall, these parasite communities were remarkably stable to perturbation. Only one non-target parasite species responded to deworming, and this response was temporary: we found strong, but short-lived, increases in the abundance of Eimeria protozoa, which share an infection site with the dominant nematode species, suggesting local, dynamic competition. These results, providing a rare and clear experimental demonstration of interactions between helminths and co-infecting parasites in wild vertebrates, constitute an important step towards understanding the wider consequences of similar drug treatments in humans and animals.

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Infection intensity over time since first capture for (a) Eimeria hungaryensis and (b) Eimeria apionodes across Ivermectin treatment groups. While E. hungaryensis infection intensity increased after each treatment, and more closely mirrored the dynamics of nematode infection probability, E. apionodes was less affected by treatment. Arrows indicate times of treatment (solid arrows denote repeated treatment; dashed arrows denote single treatment); single-treatment mice (dashed line, filled squares) are grouped with repeated treatment mice (solid line, filled circles) until four weeks, at which point they become different. Data are means and s.e.m. from raw data.
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RSPB20130598F2: Infection intensity over time since first capture for (a) Eimeria hungaryensis and (b) Eimeria apionodes across Ivermectin treatment groups. While E. hungaryensis infection intensity increased after each treatment, and more closely mirrored the dynamics of nematode infection probability, E. apionodes was less affected by treatment. Arrows indicate times of treatment (solid arrows denote repeated treatment; dashed arrows denote single treatment); single-treatment mice (dashed line, filled squares) are grouped with repeated treatment mice (solid line, filled circles) until four weeks, at which point they become different. Data are means and s.e.m. from raw data.

Mentions: Examining the Eimeria intensity response in more detail, we found evidence for species-specificity in this effect. Two species of Eimeria, differing in their infection site within the gut, are common in these wood mouse populations: E. hungaryensis and E. apionodes. Eimeria hungaryensis is found in the anterior half of the small intestine (where H. polygyrus, the most common nematode in these mice, resides; table 1) and predominantly infects enterocytes on the apex of villi, whereas E. apionodes inhabits a more posterior position in the gut, infecting enterocytes on the sides of villi or in crypts [30]. Ivermectin-treated mice showed a stronger increase in E. hungaryensis infection intensity than in E. apionodes intensity (one to three weeks after last treatment, effect of drug for E. hungaryensis: F1,12 = 13.66, p = 0.003, E. apionodes: F1,11 = 6.74, p = 0.025), and the dynamics of E. hungaryensis intensity mirrored those of nematode infection probability far more closely than the dynamics of E. apionodes (compare figure 2 with figure 1b).FigureĀ 2.


Stability of within-host-parasite communities in a wild mammal system.

Knowles SC, Fenton A, Petchey OL, Jones TR, Barber R, Pedersen AB - Proc. Biol. Sci. (2013)

Infection intensity over time since first capture for (a) Eimeria hungaryensis and (b) Eimeria apionodes across Ivermectin treatment groups. While E. hungaryensis infection intensity increased after each treatment, and more closely mirrored the dynamics of nematode infection probability, E. apionodes was less affected by treatment. Arrows indicate times of treatment (solid arrows denote repeated treatment; dashed arrows denote single treatment); single-treatment mice (dashed line, filled squares) are grouped with repeated treatment mice (solid line, filled circles) until four weeks, at which point they become different. Data are means and s.e.m. from raw data.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3673050&req=5

RSPB20130598F2: Infection intensity over time since first capture for (a) Eimeria hungaryensis and (b) Eimeria apionodes across Ivermectin treatment groups. While E. hungaryensis infection intensity increased after each treatment, and more closely mirrored the dynamics of nematode infection probability, E. apionodes was less affected by treatment. Arrows indicate times of treatment (solid arrows denote repeated treatment; dashed arrows denote single treatment); single-treatment mice (dashed line, filled squares) are grouped with repeated treatment mice (solid line, filled circles) until four weeks, at which point they become different. Data are means and s.e.m. from raw data.
Mentions: Examining the Eimeria intensity response in more detail, we found evidence for species-specificity in this effect. Two species of Eimeria, differing in their infection site within the gut, are common in these wood mouse populations: E. hungaryensis and E. apionodes. Eimeria hungaryensis is found in the anterior half of the small intestine (where H. polygyrus, the most common nematode in these mice, resides; table 1) and predominantly infects enterocytes on the apex of villi, whereas E. apionodes inhabits a more posterior position in the gut, infecting enterocytes on the sides of villi or in crypts [30]. Ivermectin-treated mice showed a stronger increase in E. hungaryensis infection intensity than in E. apionodes intensity (one to three weeks after last treatment, effect of drug for E. hungaryensis: F1,12 = 13.66, p = 0.003, E. apionodes: F1,11 = 6.74, p = 0.025), and the dynamics of E. hungaryensis intensity mirrored those of nematode infection probability far more closely than the dynamics of E. apionodes (compare figure 2 with figure 1b).FigureĀ 2.

Bottom Line: Overall, these parasite communities were remarkably stable to perturbation.Only one non-target parasite species responded to deworming, and this response was temporary: we found strong, but short-lived, increases in the abundance of Eimeria protozoa, which share an infection site with the dominant nematode species, suggesting local, dynamic competition.These results, providing a rare and clear experimental demonstration of interactions between helminths and co-infecting parasites in wild vertebrates, constitute an important step towards understanding the wider consequences of similar drug treatments in humans and animals.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Biology, and Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK. s.knowles@imperial.ac.uk

ABSTRACT
Simultaneous infection by multiple parasite species is ubiquitous in nature. Interactions among co-infecting parasites may have important consequences for disease severity, transmission and community-level responses to perturbations. However, our current view of parasite interactions in nature comes primarily from observational studies, which may be unreliable at detecting interactions. We performed a perturbation experiment in wild mice, by using an anthelminthic to suppress nematodes, and monitored the consequences for other parasite species. Overall, these parasite communities were remarkably stable to perturbation. Only one non-target parasite species responded to deworming, and this response was temporary: we found strong, but short-lived, increases in the abundance of Eimeria protozoa, which share an infection site with the dominant nematode species, suggesting local, dynamic competition. These results, providing a rare and clear experimental demonstration of interactions between helminths and co-infecting parasites in wild vertebrates, constitute an important step towards understanding the wider consequences of similar drug treatments in humans and animals.

Show MeSH
Related in: MedlinePlus