Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.

The immune system provides vital protection against pathogens, but extensive evidence suggests that mounting immune responses can entail survival and fecundity costs. The physiological mechanisms that underpin these costs remain poorly understood, despite their potentially important role in shaping...

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Main Authors: Dominic L Cram, Jonathan D Blount, Jennifer E York, Andrew J Young
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0122421
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author Dominic L Cram
Jonathan D Blount
Jennifer E York
Andrew J Young
author_facet Dominic L Cram
Jonathan D Blount
Jennifer E York
Andrew J Young
author_sort Dominic L Cram
collection DOAJ
description The immune system provides vital protection against pathogens, but extensive evidence suggests that mounting immune responses can entail survival and fecundity costs. The physiological mechanisms that underpin these costs remain poorly understood, despite their potentially important role in shaping life-histories. Recent studies involving laboratory models highlight the possibility that oxidative stress could mediate these costs, as immune-activation can increase the production of reactive oxygen species leading to oxidative stress. However, this hypothesis has rarely been tested in free-ranging wild populations, where natural oxidative statuses and compensatory strategies may moderate immune responses and their impacts on oxidative status. Furthermore, the possibility that individuals scale their immune responses according to their oxidative status, conceivably to mitigate such costs, remains virtually unexplored. Here, we experimentally investigate the effects of a phytohaemagglutinin (PHA) immune-challenge on oxidative status in wild male and female white-browed sparrow weavers, Plocepasser mahali. We also establish whether baseline oxidative status prior to challenge predicts the scale of the immune responses. Contrary to previous work on captive animals, our findings suggest that PHA-induced immune-activation does not elicit oxidative stress. Compared with controls (n = 25 birds), PHA-injected birds (n = 27 birds) showed no evidence of a differential change in markers of oxidative damage or enzymatic and non-enzymatic antioxidant protection 24 hours after challenge. We did, however, find that the activity of a key antioxidant enzyme (superoxide dismutase, SOD) prior to immune-activation predicted the scale of the resulting swelling: birds with stronger initial SOD activity subsequently produced smaller swellings. Our findings (i) suggest that wild birds can mount immune responses without suffering from systemic oxidative stress, and (ii) lend support to biomedical evidence that baseline oxidative status can impact the scale of immune responses; a possibility not yet recognised in ecological studies of immunity.
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spelling doaj-art-bc1ea4f30d5041bca44742f106d1c8122025-08-20T03:10:06ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01103e012242110.1371/journal.pone.0122421Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.Dominic L CramJonathan D BlountJennifer E YorkAndrew J YoungThe immune system provides vital protection against pathogens, but extensive evidence suggests that mounting immune responses can entail survival and fecundity costs. The physiological mechanisms that underpin these costs remain poorly understood, despite their potentially important role in shaping life-histories. Recent studies involving laboratory models highlight the possibility that oxidative stress could mediate these costs, as immune-activation can increase the production of reactive oxygen species leading to oxidative stress. However, this hypothesis has rarely been tested in free-ranging wild populations, where natural oxidative statuses and compensatory strategies may moderate immune responses and their impacts on oxidative status. Furthermore, the possibility that individuals scale their immune responses according to their oxidative status, conceivably to mitigate such costs, remains virtually unexplored. Here, we experimentally investigate the effects of a phytohaemagglutinin (PHA) immune-challenge on oxidative status in wild male and female white-browed sparrow weavers, Plocepasser mahali. We also establish whether baseline oxidative status prior to challenge predicts the scale of the immune responses. Contrary to previous work on captive animals, our findings suggest that PHA-induced immune-activation does not elicit oxidative stress. Compared with controls (n = 25 birds), PHA-injected birds (n = 27 birds) showed no evidence of a differential change in markers of oxidative damage or enzymatic and non-enzymatic antioxidant protection 24 hours after challenge. We did, however, find that the activity of a key antioxidant enzyme (superoxide dismutase, SOD) prior to immune-activation predicted the scale of the resulting swelling: birds with stronger initial SOD activity subsequently produced smaller swellings. Our findings (i) suggest that wild birds can mount immune responses without suffering from systemic oxidative stress, and (ii) lend support to biomedical evidence that baseline oxidative status can impact the scale of immune responses; a possibility not yet recognised in ecological studies of immunity.https://doi.org/10.1371/journal.pone.0122421
spellingShingle Dominic L Cram
Jonathan D Blount
Jennifer E York
Andrew J Young
Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.
PLoS ONE
title Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.
title_full Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.
title_fullStr Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.
title_full_unstemmed Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.
title_short Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.
title_sort immune response in a wild bird is predicted by oxidative status but does not cause oxidative stress
url https://doi.org/10.1371/journal.pone.0122421
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