Thermoregulatory costs of the innate immune response are modulated by winter food availability in a small passerine
(2023) In Journal of Animal Ecology 92(5). p.1065-1074- Abstract
In winter, a challenge to the immune system could pose a major energetic trade-off for small endotherms, whereby increasing body temperature (Tb; i.e. eliciting fever) may be beneficial to fight off invading pathogens yet incur a cost for vital energy-saving mechanisms. Having previously shown that the availability and acquisition of energy, through manipulation of food predictability, influences the depth of rest-phase hypothermia in a wild bird in winter, we expected that the nocturnal thermoregulatory component of the acute-phase immune response would also be modulated by food availability. By manipulating winter food availability in the wild for great tits Parus major, we created an area offering a “predictable” and... (More)
In winter, a challenge to the immune system could pose a major energetic trade-off for small endotherms, whereby increasing body temperature (Tb; i.e. eliciting fever) may be beneficial to fight off invading pathogens yet incur a cost for vital energy-saving mechanisms. Having previously shown that the availability and acquisition of energy, through manipulation of food predictability, influences the depth of rest-phase hypothermia in a wild bird in winter, we expected that the nocturnal thermoregulatory component of the acute-phase immune response would also be modulated by food availability. By manipulating winter food availability in the wild for great tits Parus major, we created an area offering a “predictable” and constant supply of food at feeding stations, while an unmanipulated area was subject to naturally “unpredictable” food. Birds were subject to an immune challenge shortly after dusk, and the thermoregulatory response was quantified via continuous recording of nocturnal Tb, using subcutaneous thermo-sensitive transponders. In response to immune challenge, all birds increased Tb above the level maintained prior to immune challenge (i.e. baseline). However, birds experiencing a naturally unpredictable food supply elevated Tb more than birds subject to predictable food resources, during the period of expected peak response and for the duration of the night. Furthermore, “unpredictable-food” females took longer to return to their baseline Tb. Assuming baseline nocturnal Tb reflects an individual's optimum, based on their available energy budget, the metabolic cost of eliciting an acute-phase response for “unpredictable-food” birds was more than double that of “predictable-food” birds. The absence of differences in absolute Tb during the peak response could support the idea of an optimal Tb for immune system activation. Alternatively, “predictable-food” birds could have acquired tolerance to endotoxin as a result of using feeding stations, thus affording them reduced costs associated with a smaller Tb increase. These findings shed new light on the trade-offs associated with food acquisition, thermoregulation and immune function in small-bodied endotherms. This knowledge is of increasing importance, given the predicted elevated pathogen risks associated with changes in climate and anthropogenic activities.
(Less)
- author
- Watson, Hannah LU ; Nilsson, Jan Åke LU and Nilsson, Johan F. LU
- organization
- publishing date
- 2023-05
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- body temperature, fever, food availability, immune response, thermoregulation, winter ecology
- in
- Journal of Animal Ecology
- volume
- 92
- issue
- 5
- pages
- 10 pages
- publisher
- Wiley-Blackwell
- external identifiers
-
- pmid:37032462
- scopus:85152291863
- ISSN
- 0021-8790
- DOI
- 10.1111/1365-2656.13914
- language
- English
- LU publication?
- yes
- id
- f0916dcd-37c0-4af7-b10c-8e1d9c08e5d6
- date added to LUP
- 2023-07-21 11:15:13
- date last changed
- 2024-04-19 23:52:44
@article{f0916dcd-37c0-4af7-b10c-8e1d9c08e5d6,
abstract = {{<p>In winter, a challenge to the immune system could pose a major energetic trade-off for small endotherms, whereby increasing body temperature (T<sub>b</sub>; i.e. eliciting fever) may be beneficial to fight off invading pathogens yet incur a cost for vital energy-saving mechanisms. Having previously shown that the availability and acquisition of energy, through manipulation of food predictability, influences the depth of rest-phase hypothermia in a wild bird in winter, we expected that the nocturnal thermoregulatory component of the acute-phase immune response would also be modulated by food availability. By manipulating winter food availability in the wild for great tits Parus major, we created an area offering a “predictable” and constant supply of food at feeding stations, while an unmanipulated area was subject to naturally “unpredictable” food. Birds were subject to an immune challenge shortly after dusk, and the thermoregulatory response was quantified via continuous recording of nocturnal T<sub>b</sub>, using subcutaneous thermo-sensitive transponders. In response to immune challenge, all birds increased T<sub>b</sub> above the level maintained prior to immune challenge (i.e. baseline). However, birds experiencing a naturally unpredictable food supply elevated T<sub>b</sub> more than birds subject to predictable food resources, during the period of expected peak response and for the duration of the night. Furthermore, “unpredictable-food” females took longer to return to their baseline T<sub>b</sub>. Assuming baseline nocturnal T<sub>b</sub> reflects an individual's optimum, based on their available energy budget, the metabolic cost of eliciting an acute-phase response for “unpredictable-food” birds was more than double that of “predictable-food” birds. The absence of differences in absolute T<sub>b</sub> during the peak response could support the idea of an optimal T<sub>b</sub> for immune system activation. Alternatively, “predictable-food” birds could have acquired tolerance to endotoxin as a result of using feeding stations, thus affording them reduced costs associated with a smaller T<sub>b</sub> increase. These findings shed new light on the trade-offs associated with food acquisition, thermoregulation and immune function in small-bodied endotherms. This knowledge is of increasing importance, given the predicted elevated pathogen risks associated with changes in climate and anthropogenic activities.</p>}},
author = {{Watson, Hannah and Nilsson, Jan Åke and Nilsson, Johan F.}},
issn = {{0021-8790}},
keywords = {{body temperature; fever; food availability; immune response; thermoregulation; winter ecology}},
language = {{eng}},
number = {{5}},
pages = {{1065--1074}},
publisher = {{Wiley-Blackwell}},
series = {{Journal of Animal Ecology}},
title = {{Thermoregulatory costs of the innate immune response are modulated by winter food availability in a small passerine}},
url = {{http://dx.doi.org/10.1111/1365-2656.13914}},
doi = {{10.1111/1365-2656.13914}},
volume = {{92}},
year = {{2023}},
}