Endotoxin injection attenuates rest‐phase hypothermia in wintering great tits through the onset of fever

Abstract

Summary1. Endothermic animals in the boreal region experience considerable thermoregulatory costs in winter, especially during inactive periods when high demands cannot be met by increased food intake. This might necessitate a trade-off between resting thermoregulation and other energetically expensive processes, such as immune function, but this has rarely been investigated. 2. We evaluated how immune activation affected rest-phase hypothermia (an important energy conservation mechanism in small animals), in wild great tits (Parus major L.) wintering under semi-natural conditions in southern Sweden. The acute phase response was triggered immediately prior to sunset through intramuscular lipopolysaccharide (LPS, an endotoxin) administration in two contrasting, naturally occurring, thermal regimes (cold, mild). We then noninvasively measured the thermoregulatory response throughout the night using subcutaneously implanted temperature-sensitive transmitters. 3. Despite the energetic benefits of hypothermia, immunized great tits displayed an attenuated hypothermic response manifested through the onset of fever, possibly at the expense of a higher sustained metabolic rate. In line with this, these birds lost more body mass overnight (but only in mild conditions) and consequently were in worse condition the subsequent morning. 4. Fever expression was remarkably similar in cold and mild conditions, despite substantial variation in the energetic cost for thermoregulation. This suggest that the degree of fever is flexible and represents a trade-off between the minimum body temperature required to mount an adequate acute phase response and the energy expenditure needed to maintain it. 5. We suggest that while energy conservation and immune function may not always be exclusive activities, costs of immune defences probably constitute an important additive energetic cost during northern winter conditions, sometimes calling for trade-offs with other important physiological processes to survive the night.

Body temperature changes during simulated bacterial infection in a songbird: fever at night and hypothermia at day

“…It has been proposed that the immune defence system might work best at a given body temperature or within a range of body temperatures (Nord et al, 2013). The occurrence of daytime hypothermia in our study could then be explained if this optimal body temperature, or body temperature range, is lower than the normal daytime body temperature.…”

“…Our data do not support the hypothesis of a single optimal temperature for immune function, in which case we would have expected all LPS-challenged birds, irrespective of dose, to maintain this body temperature during the acute phase response (cf. discussion in Nord et al, 2013). However, treatment-wise differences in body temperature were relatively small when integrated over the duration of the response.…”

“…While we did not assess the dose-response to LPS at night, the magnitude of fever is proportional to LPS dose in fowl (e.g. Jones et al, 1983;Maloney and Gray, 1998), and great tits (Parus major) challenged with LPS in winter maintained similar febrile body temperatures regardless of variation in ambient temperature (Nord et al, 2013). This supports the view that fever in birds might represent a trade-off between optimal immune function and the energy costs of the immune response, and that proper immune function can only be realized within a certain range of body temperatures (see discussion on optimal body temperatures for the immune system, above).…”

“…Even in response to a challenge with similar or identical doses of the same artificial endotoxin, large nonpasserine birds such as fowl typically demonstrate fever (Maloney and Gray, 1998;Koutsos and Klasing, 2001;Leshchinsky and Klasing, 2001;Marais et al, 2011a), whereas small passerines sometimes respond with fever (Adelman et al, 2010a,b;Coon et al, 2011;Nord et al, 2013) and sometimes with hypothermia (Owen- Ashley et al, 2006;Burness et al, 2010;King and Swanson, 2013), the latter being observed more often during the day (but see Adelman et al, 2010b). The reasons for this variation in the body temperature response to an endotoxin challenge among small passerine birds, and between small and large (e.g.…”

“…We further expected body temperature changes to be mirrored by changes in food intake, body mass gain and overnight body mass loss (the last of these being attenuated for doses that resulted in the use of hypothermia where energy costs of the immune response should be lower). Two months after the first experiment, we administered a single, moderately strong, dose of LPS (that has previously been used to trigger nocturnal fever in passerines; Nord et al, 2013) in the evening and measured the body temperature response and body mass loss at night, in order to study any variation in these responses that could be related to the circadian timing of the challenge. We predicted that the nocturnal fever response and associated body mass loss should be similar to those observed during the day, which would be compatible with the notion that endotoxin-induced hypothermia develops only during severe infection or sepsis.…”