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Biologging in a free-ranging mammal reveals apparent energetic trade-offs among physiological and behavioural components of the acute-phase response

The Royal Society
Biology Letters
Authors:
Austin Z T Allison
Austin Z T Allison
Austin Z T Allison
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Helen Chmura at US Forest Service
Helen Chmura
Cory Williams at Colorado State University
Cory Williams
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Abstract

The acute-phase response (APR) is an adaptive emergency life-history stage, wherein vertebrates exhibit fever and anorexia to survive an infection. However, induced immune responses are energetically costly, and sick animals may reduce physical activity to compensate. Tests of this predicted energetic trade-off in free-ranging animals are rare due to difficulties in measuring individual physiology and behaviour under immune challenge in natural settings. However, recent advances in biologging technology now make such studies possible. We surgically implanted heart rate/temperature loggers in free-ranging adult male Arctic ground squirrels, fitted the squirrels with collar-mounted accelerometers and light/temperature loggers, and injected animals with lipopolysaccharide (LPS) to simulate an immune challenge. LPS-injected squirrels exhibited approximately 1°C overnight fevers accompanied by slightly elevated (10 bpm) heart rates; LPS-injected squirrels also spent 19% less of their time aboveground the following day and reduced overall movement by 40% compared with saline-injected controls. Thus, we found support for an energetic trade-off between functional immune responses (fever and anorexia) and lethargic sickness behaviour within the APR of a free-ranging mammal. Moreover, our results suggest animal-borne devices can play an important role in future studies of vertebrate immunity and disease dynamics.
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Biologging in a free-ranging mammal
reveals apparent energetic trade-offs
among physiological and behavioural
components of the acute-phase response
Austin Z. T. Allison1, Helen E. Chmura2 and Cory T. Williams1
1Department of Biology, Colorado State University, 1878 Campus Delivery, Fort Collins, CO 80523, USA
2Rocky Mountain Research Station, U.S. Forest Service, 800 E. Beckwith Ave, Missoula, MT 59801, USA
AZTA,0000-0002-0786-5352; HEC,0000-0001-6626-8534
The acute-phase response (APR) is an adaptive emergency life-history
stage, wherein vertebrates exhibit fever and anorexia to survive
an infection. However, induced immune responses are energetically
costly, and sick animals may reduce physical activity to compensate.
Tests of this predicted energetic trade-off in free-ranging animals
are rare due to difficulties in measuring individual physiology and
behaviour under immune challenge in natural settings. However, recent
advances in biologging technology now make such studies possible. We
surgically implanted heart rate/temperature loggers in free-ranging adult
male Arctic ground squirrels, fitted the squirrels with collar-mounted
accelerometers and light/temperature loggers, and injected animals with
lipopolysaccharide (LPS) to simulate an immune challenge. LPS-injected
squirrels exhibited approximately 1°C overnight fevers accompanied by
slightly elevated (10 bpm) heart rates; LPS-injected squirrels also spent
19% less of their time aboveground the following day and reduced overall
movement by 40% compared with saline-injected controls. Thus, we found
support for an energetic trade-off between functional immune responses
(fever and anorexia) and lethargic sickness behaviour within the APR of a
free-ranging mammal. Moreover, our results suggest animal-borne devices
can play an important role in future studies of vertebrate immunity and
disease dynamics.
1. Introduction
Disease and parasitism are strong agents of selection that shape the evolu-
tion of physiological and behavioural immune responses in animals. The
acute-phase response (APR), for instance, constitutes an adaptive emer-
gency life-history stage that is evolutionarily conserved across vertebrate
lineages [1–4]. This non-specific response to infection often includes eleva-
ted body temperature (fever) and increased production of certain proteins
to inhibit pathogenic propagation [5]. However, these physiological altera-
tions are energetically costly [6–8]. Moreover, the APR frequently involves
reduced food intake (anorexia) to deprive pathogens of nutrients required
for reproduction [1,9,10]. To compensate for reduced energetic intake and/or
increased energetic expenditure, animals undergoing an APR may exhibit
lethargy [1,10]. Hence, the APR apparently sacrifices short-term growth and
reproductive opportunities to maximize the odds of surviving an infection
and so conserve future reproductive opportunities [11–14].
The APR is well documented in domesticated animals and laboratory
settings—especially in birds and mammals [15–18]—but relatively few studies
have considered fever and sickness behaviour in free-ranging animals [19–
© 2024 The Author(s). Published by the Royal Society. All rights reserved.
Research
Cite this article: Allison AZT, Chmura HE,
Williams CT. 2024 Biologging in a free-ranging
mammal reveals apparent energetic trade-offs
among physiological and behavioural
components of the acute-phase response. Biol.
Lett. 20: 20240437.
https://doi.org/10.1098/rsbl.2024.0437
Received: 28 July 2024
Accepted: 16 October 2024
Subject Category:
Animal behaviour
Subject Areas:
behaviour, ecology, evolution
Keywords:
accelerometer, fever, geolocator, heart rate,
immune challenge, sickness behaviour
Author for correspondence:
Austin Z. T. Allison
e-mail: austin.allison@colostate.edu
Electronic supplementary material is available
online at https://doi.org/10.6084/
m9.figshare.c.7562130.
ResearchGate has not been able to resolve any citations for this publication.
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