Measuring body temperature in birds - the effects of sensor type and placement on estimated temperature and metabolic rate.

Several methods are routinely used to measure avian body temperature, but different methods vary in invasiveness. This may cause stress-induced increases in temperature and/or metabolic rate and, hence, overestimation of both parameters. Choosing an adequate temperature measurement method is therefore key to accurately characterizing an animal's thermal and metabolic phenotype. Using great tits (Parus major) and four common methods with different levels of invasiveness (intraperitoneal, cloacal, subcutaneous, cutaneous), we evaluated the preciseness of body temperature measurements and effects on resting metabolic rate (RMR) over a 40°C range of ambient temperatures. None of the methods caused overestimation or underestimation of RMR compared with un-instrumented birds, and body or skin temperature estimates did not differ between methods in thermoneutrality. However, skin temperature was lower compared with all other methods below thermoneutrality. These results provide empirical guidance for future research that aims to measure body temperature and metabolic rate in small bird models.

Variation in breeding phenology in response to climate change in two passerine species.

Increasingly warmer springs have caused phenological shifts in both plants and animals. In birds, it is well established that mean laying date has advanced to match the earlier food peak. We know less about changes in the distribution of egg-laying dates within a population and the environmental variables that determine this variation. This could be an important component of how populations respond to climate change. We, therefore, used laying date and environmental data from 39 years (1983-2021) to determine how climate change affected laying date variation in blue tits (Cyanistes caeruleus) and marsh tits (Poecile palustris), two sympatric passerines with different life histories. Both species advanced mean laying date (0.19-0.24 days per year) and mean laying date showed a negative relationship with maximum spring temperature in both blue and marsh tits. In springs with no clear temperature increase during the critical time window (the time-window in which mean laying date was most sensitive to temperature) start of breeding in blue tits was distributed over a longer part of the season. However, there was no such pattern in marsh tits. Our findings suggest that temperature change, and not necessarily absolute temperature, can shape the variation in breeding phenology in a species-specific manner, possibly linked to variation in life-history strategies. This is an important consideration when predicting how climate change affects timing of breeding within a population.

Thyroid function and immune status in perch (Perca fluviatilis) from lakes contaminated with PFASs or PCBs.

The environment contains a multitude of man-made chemicals, some of which can act as endocrine disruptors (EDCs), while others can be immunotoxic. We evaluated thyroid disruption and immunotoxic effects in wild female perch (Perca fluviatilis) collected from two contaminated areas in Sweden; one site contaminated with per- and polyfluoroalkyl substances (PFASs) and two sites contaminated with polychlorinated biphenyls (PCBs), with one reference site included for each area. The hepatic mRNA expression of thyroid receptors α and ß, and the thyroid hormone metabolising iodothyronine deiodinases (dio1, dio2 and dio3) were measured using real-time PCR, while the levels of thyroid hormone T3 in plasma was analysed using a radioimmunoassay. In addition, lymphocytes, granulocytes, and thrombocytes were counted microscopically. Our results showed lower levels of T3 as well as lower amounts of lymphocytes and granulocytes in perch collected from the PFAS-contaminated site compared to reference sites. In addition, expressions of mRNA coding for thyroid hormone metabolising enzymes (dio2 and dio3) and thyroid receptor α (thra) were significantly different in these fish compared to their reference site. For perch collected at the two PCB-contaminated sites, there were no significant differences in T3 levels or in expression levels of the thyroid-related genes, compared to the reference fish. Fish from one of the PCB-contaminated sites had higher levels of thrombocytes compared with both the second PCB lake and their reference lake; hence PCBs are unlikely to be the cause of this effect. The current study suggests that lifelong exposure to PFASs could affect both the thyroid hormone status and immune defence of perch in the wild.

Experimental facilitation of heat loss affects work rate and innate immune function in a breeding passerine bird.

The capacity to get rid of excess heat produced during hard work is a possible constraint on parental effort during reproduction [heat dissipation limit (HDL) theory]. We released hard-working blue tits (Cyanistes caeruleus) from this constraint by experimentally removing ventral plumage. We then assessed whether this changed their reproductive effort (feeding rate and nestling size) and levels of self-maintenance (change in body mass and innate immune function). Feather-clipped females reduced the number of feeding visits and increased levels of constitutive innate immunity compared with unclipped females but did not fledge smaller nestlings. Thus, they increased self-maintenance without compromising current reproductive output. In contrast, feather clipping did not affect the number of feeding visits or innate immune function in males, despite increased heat loss rate. Our results show that analyses of physiological parameters, such as constitutive innate immune function, can be important when trying to understand sources of variation in investment in self-maintenance versus reproductive effort and that risk of overheating can influence innate immune function during reproduction.

Deep body and surface temperature responses to hot and cold environments in the zebra finch.

Global warming increasingly challenges thermoregulation in endothermic animals, particularly in hot and dry environments where low water availability and high temperature increase the risk of hyperthermia. In birds, un-feathered body parts such as the head and bill work as 'thermal windows', because heat flux is higher compared to more insulated body regions. We studied how such structures were used in different thermal environments, and if heat flux properties change with time in a given temperature. We acclimated zebra finches (Taeniopygia guttata) to two different ambient temperatures, 'cold' (5 °C) and 'hot' (35 °C), and measured the response in core body temperature using a thermometer, and head surface temperature using thermal imaging. Birds in the hot treatment had 10.3 °C higher head temperature than those in the cold treatment. Thermal acclimation also resulted in heat storage in the hot group: core body temperature was 1.1 °C higher in the 35 °C group compared to the 5 °C group. Hence, the thermal gradient from core to shell was 9.03 °C smaller in the hot treatment. Dry heat transfer rate from the head was significantly lower in the hot compared to the cold treatment after four weeks of thermal acclimation. This reflects constraints on changes to peripheral circulation and maximum body temperature. Heat dissipation capacity from the head region increased with acclimation time in the hot treatment, perhaps because angiogenesis was required to reach peak heat transfer rate. We have shown that zebra finches meet high environmental temperature by heat storage, which saves water and energy, and by peripheral vasodilation in the head, which facilitates dry heat loss. These responses will not exclude the need for evaporative cooling, but will lessen the amount of energy expend on body temperature reduction in hot environments.

Age-dependent effects of predation risk on night-time hypothermia in two wintering passerine species.

Small animals that winter at northern latitudes need to maximize energy intake and minimize energy loss. Many passerine birds use night-time hypothermia to conserve energy. A potential cost of night-time hypothermia with much theoretical (but little empirical) support is increased risk of night-time predation, due to reduced vigilance and lower escape speed in hypothermic birds. This idea has never been tested in the wild. We, therefore, increased perceived predation risk in great tits (Parus major) and blue tits (Cyanistes caeruleus) roosting in nest boxes during cold winter nights to measure any resultant effect on their use of night-time hypothermia. Roosting birds of both species that experienced their first winter were less prone to use hypothermia as an energy-saving strategy at low ambient temperatures when exposed to increased perceived predation risk either via handling (great tits) or via predator scent manipulation (blue tits). However, we did not record such effects in birds that were in their second winter or beyond. Our results suggest that effects of increased predation risk are age- and temperature specific. This could be caused by age-related differences in experience and subsequent risk assessment, or by dominance-related variation in habitat quality between young and old birds. Predation risk could, through its effect on use and depth of night-time hypothermia, be important for total energy management and winter survival for resident birds at northern latitudes.

Brood size constrains the development of endothermy in blue tits.

Altricial birds are unable to maintain body temperature when exposed to low ambient temperatures during the first days after hatching. Thermoregulatory capacity begins to form as postnatal development progresses, and eventually nestlings become homeothermic. Several factors may influence this development at both the level of the individual and the level of the whole brood, but to our knowledge no studies have focused on the effect of brood size per se on the development of endothermy in individual nestlings. We performed cooling experiments on blue tit (Cyanistes caeruleus) nestlings in the field, to study how different experimental brood sizes affected the development of endothermy in individual nestlings and the thermal environment experienced by the whole brood in the nest. Nestlings from all experimental brood sizes showed a decrease in cooling rate as they grew older, but birds from reduced broods showed an earlier onset of endothermy compared with nestlings from enlarged and control broods. This difference manifested during early development and gradually disappeared as nestlings grew older. The thermal environment in the nests differed between treatments during nestling development, such that nest temperature in reduced broods was lower than that in enlarged broods during all days and during nights at the end of the experimental period. We suggest that the development of endothermy in blue tit nestlings is not ontogenetically fixed, but instead may vary according to differences in developmental, nutritional and thermal conditions as determined by brood size.

Age differences in night-time metabolic rate and body temperature in a small passerine.

Spending the winter in northern climes with short days and cold ambient temperatures (Ta) can be energetically challenging for small birds that have high metabolic and heat loss rates. Hence, maintaining body temperature (Tb) in Ta below thermoneutrality can be energetically costly for a small bird. We still know little about how increased heat production below thermoneutrality affects the level at which Tb is maintained, and if these patterns are age specific. To test this, we measured subcutaneous body temperature (Ts) and resting metabolic rate (RMR) simultaneously in blue tits (Cyanistes caeruleus) during winter nights in Ta's ranging from 25 to - 15 °C. RMR increased below the lower critical temperature (LCT, estimated at 14 °C) and was 6% higher in young (birds in their first winter) compared to old birds (birds in their second winter or older). The higher RMR was also mirrored in higher Ts and thermal conductance (C) in young birds, which we suggest could be caused by age differences in plumage quality, likely driven by time constraints during moult. Reduction in nightly predicted Tb was modest and increased again at the coldest ambient temperatures, suggesting that either heat retention or heat production (or both) improved when Ta reached levels which are cold by the standards of birds in our population. Our results show that levels of heat production and Tb can be age specific. Further studies should address age-specific differences on quality, structure, and thermal conductivity of plumage more explicitly, to investigate the role of variation in insulation in age-linked metabolic phenotypes.