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

Abstract

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.

A Potent Anti-Inflammatory Response in Bat Macrophages May Be Linked to Extended Longevity and Viral Tolerance

“…Interestingly, wild caught Molossus molossus bats injected with LPS showed no leucocytosis or fever (Stockmaier et al, 2015), which could be hypotheticaly explained by increased levels of antipyretic Il-10. However this observation might be speciesor experimental set-up-specific, as LPS induced fever was observed in Myotis vivesi (Otálora-Ardila et al, 2016) and leukocytosis occurred in challenged Carollia perspicillata (Schneeberger et al, 2013); therefore the LPS induced systemic responses in bats require further investigation. The proposed link between bat longevity, viral tolerance and antiinflammatory response is certainly plausible also in the light of available evidence from other species.…”

Going to Bat(s) for Studies of Disease Tolerance

“…In addition to general studies of immune cell recruitment and transcriptional responses during WNS, body mass and white blood cell counts were examined following LPS administration in four bat species (134)(135)(136)(137). Subcutaneous LPS challenge in of Pallas's mastiff bats (Molossus molossus) led to a loss of body mass of ∼7% within the first day, but did not result in changes in circulating white blood cell counts or body temperature (135).…”

“…Seba's short-tailed fruit bat (Carollia perspicillata) also showed a decrease in body mass following LPS challenge, but this was associated with increases in white blood cell counts as well as increases in derivatives of reactive oxidative metabolites (dROM) (134). Subdermal LPS challenge of fish-eating Myotis (Myotis vivesi) led to body mass decreases, increased resting metabolic rate and skin temperature (136), while intraperitoneal LPS challenge of wrinkle-lipped bats (Chaerephon plicatus) caused an increase in circulating leukocytes, but did not result in a reduction in body mass compared to controls (137). The differential responses to LPS challenge suggest that the immune response to bacterial infection varies across species.…”

Peer Review #2 of "The energetic cost of mounting an immune response for Pallas’s long-tongued bat (Glossophaga soricina) (v0.2)"

“…The metabolic cost of this short-term (within 24 hours after LPS injection) APR has been measured for a handful of species with contrasting results. APR activation resulted in a large increase (185%) in RMR for fish-eating Myotis (Myotis vivesi; Otálora-Ardila et al, 2016, 2017, a modest increase (~26-40%) for Pekin ducks (Anas platyrhynchos; Marais, Maloney & Gray, 2011) and house sparrows (Passer domesticus; King & PeerJ reviewing PDF | (2017:10:21237:2:0:NEW 14 Mar 2018)…”

“…Manuscript to be reviewed Swanson, 2013;Martin et al, 2017), a small increase (~10-14%) for zebra finches (Taeniopygia guttata; Burness, Armstrong & Tilman-Schindel, 2010), house sparrows (Martin et al, 2017) and the brown rat (Rattus norvegicus;MacDonald et al, 2012), and null increase for zebra finches (Sköld-Chiriac et al, 2014), house sparrows (Martin et al, 2017) and house mice (Mus musculus; Baze, Hunter & Hayes, 2011). These studies involved both captive-raised (Burness, Armstrong & Tilman-Schindel, 2010;Baze, Hunter & Hayes, 2011;Marais, Maloney & Gray, 2011;Sköld-Chiriac et al, 2014) and wild populations (King & Swanson 2013, Otálora-Ardila et al 2016, 2017, Martin et al, 2017 A strong immune response is assumed to be more likely for long-lived animals (Lochmiller & Deerenberg, 2000), such as bats. Bats are one of the most diverse orders of vertebrates both in taxonomic and ecological terms and thus represent an exceptional model to test if APR is an energetically costly event.…”