Does the strength of an immune response reflect its energetic cost?

Nilsson, Jan‐Åke; Granbom, Martin; Råberg, Lars

doi:10.1111/j.0908-8857.2007.03919.x

Cited by 41 publications

(23 citation statements)

References 41 publications

(37 reference statements)

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“…The increase in nightly metabolic rate, BMR and body temperature fall within the expected costs of fever [64]. The average increase in metabolic rate (regardless of stage) was similar to the increases reported in other studies after immune challenges in single annual cycle stages [4], [12], [65], [66]. Thus, inflammation-associated metabolic costs may be fairly conserved among avian species and not simply consistent among annual cycle stages within skylarks.…”

Section: Discussionsupporting

confidence: 83%

Wild Skylarks Seasonally Modulate Energy Budgets but Maintain Energetically Costly Inflammatory Immune Responses throughout the Annual Cycle

et al. 2012

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A central hypothesis of ecological immunology is that immune defences are traded off against competing physiological and behavioural processes. During energetically demanding periods, birds are predicted to switch from expensive inflammatory responses to less costly immune responses. Acute phase responses (APRs) are a particularly costly form of immune defence, and, hence, seasonal modulations in APRs are expected. Yet, hypotheses about APR modulation remain untested in free-living organisms throughout a complete annual cycle. We studied seasonal modulations in the APRs and in the energy budgets of skylarks Alauda arvensis, a partial migrant bird from temperate zones that experiences substantial ecological changes during its annual cycle. We characterized throughout the annual cycle changes in their energy budgets by measuring basal metabolic rate (BMR) and body mass. We quantified APRs by measuring the effects of a lipopolysaccharide injection on metabolic rate, body mass, body temperature, and concentrations of glucose and ketone. Body mass and BMR were lowest during breeding, highest during winter and intermediate during spring migration, moult and autumn migration. Despite this variation in energy budgets, the magnitude of the APR, as measured by all variables, was similar in all annual cycle stages. Thus, while we find evidence that some annual cycle stages are relatively more energetically constrained, we find no support for the hypothesis that during these annual cycle stages birds compromise an immune defence that is itself energetically costly. We suggest that the ability to mount an APR may be so essential to survival in every annual cycle stage that skylarks do not trade off this costly form of defence with other annual cycle demands.

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Section: Discussionsupporting

confidence: 83%

Wild Skylarks Seasonally Modulate Energy Budgets but Maintain Energetically Costly Inflammatory Immune Responses throughout the Annual Cycle

et al. 2012

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“…Experimental work in homeothermic vertebrates indicates that the effects of PHA and LPS application on metabolic rate are not uniform. For example, PHA administration has been shown to induce large (30%) [15] or small increases in resting metabolic rate (RMR) in some organisms (~5%) [16], no increases in RMR [17–21], and even decreases in RMR in others (-20‒-25%) [18]. Similarly, the effect of LPS administration on vertebrate RMR varies from large (~33‒40%) [22, 23] to small (~10%) [24–26] or null [27, 28].…”

Section: Introductionmentioning

confidence: 99%

Metabolic Cost of the Activation of Immune Response in the Fish-Eating Myotis (Myotis vivesi): The Effects of Inflammation and the Acute Phase Response

2016

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Inflammation and activation of the acute phase response (APR) are energetically demanding processes that protect against pathogens. Phytohaemagglutinin (PHA) and lipopolysaccharide (LPS) are antigens commonly used to stimulate inflammation and the APR, respectively. We tested the hypothesis that the APR after an LPS challenge was energetically more costly than the inflammatory response after a PHA challenge in the fish-eating Myotis bat (Myotis vivesi). We measured resting metabolic rate (RMR) after bats were administered PHA and LPS. We also measured skin temperature (Tskin) after the LPS challenge and skin swelling after the PHA challenge. Injection of PHA elicited swelling that lasted for several days but changes in RMR and body mass were not significant. LPS injection produced a significant increase in Tskin and in RMR, and significant body mass loss. RMR after LPS injection increased by 140–185% and the total cost of the response was 6.50 kJ. Inflammation was an energetically low-cost process but the APR entailed a significant energetic investment. Examination of APR in other bats suggests that the way in which bats deal with infections might not be uniform.

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“…Previous studies quantifying the energetic cost of immunity have focused on measuring changes in basal metabolic rates following immune challenge [9, 16, 17]. Basal (or resting when measured under less restrictive circumstances) metabolic rates reflect the rate of ATP hydrolysis required to maintain cellular processes during physical inactivity [18].…”

Section: Introductionmentioning

confidence: 99%

Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion

2016

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Energy-based trade-offs occur when investment in one fitness-related trait diverts energy away from other traits. The extent to which such trade-offs are shaped by limits on the rate of conversion of energy ingested in food (e.g. carbohydrates) into chemical energy (ATP) by oxidative metabolism rather than by the amount of food ingested in the first place is, however, unclear. Here we tested whether the ATP required for mounting an immune response will lead to a trade-off with ATP available for physical activity in mosquitofish (Gambusia holbrooki). To this end, we challenged fish either with lipopolysaccharide (LPS) from E. coli or with Sheep Red Blood Cells (SRBC), and measured oxygen consumption at rest and during swimming at maximum speed 24h, 48h and 7 days post-challenge in order to estimate metabolic rates. Relative to saline-injected controls, only LPS-injected fish showed a significantly greater resting metabolic rate two days post-challenge and significantly higher maximal metabolic rates two and seven days post-challenge. This resulted in a significantly greater metabolic scope two days post-challenge, with LPS-fish transiently overcompensating by increasing maximal ATP production more than would be required for swimming in the absence of an immune challenge. LPS-challenged fish therefore increased their production of ATP to compensate physiologically for the energetic requirements of immune functioning. This response would avoid ATP shortages and allow fish to engage in an aerobically-challenging activity (swimming) even when simultaneously mounting an immune response. Nevertheless, relative to controls, both LPS- and SRBC-fish displayed reduced body mass gain one week post-injection, and LPS-fish actually lost mass. The concomitant increase in metabolic scope and reduced body mass gain of LPS-challenged fish indicates that immune-associated trade-offs are not likely to be shaped by limited oxidative metabolic capacities, but may instead result from limitations in the acquisition, assimilation or efficient use of resources.

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Does the strength of an immune response reflect its energetic cost?

Cited by 41 publications

References 41 publications

Wild Skylarks Seasonally Modulate Energy Budgets but Maintain Energetically Costly Inflammatory Immune Responses throughout the Annual Cycle

Wild Skylarks Seasonally Modulate Energy Budgets but Maintain Energetically Costly Inflammatory Immune Responses throughout the Annual Cycle

Metabolic Cost of the Activation of Immune Response in the Fish-Eating Myotis (Myotis vivesi): The Effects of Inflammation and the Acute Phase Response

Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion

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