Seasonal effects on thermoregulatory responses of the Rock Kestrel, Falco rupicolis

Thermoregulatory responses are known to differ seasonally in endotherms and this is often dependent on the environment and region they are resident. Holarctic animals are exposed to severe winters and substantial seasonal variation in ambient temperature. In contrast, those in the Afrotropics have less severe winters, but greater variation in temperature, rainfall and net primary production. These environmental factors place different selection pressures on physiological responses in endotherms. In this study, metabolic rate (VO₂) and body temperature (T_b) were measured in captive bred Rock Kestrels (Falco rupicolus) from the Afrotropics after a period of summer and winter acclimatisation. Resting metabolic rate was significantly lower after the winter acclimatisation period than after the summer acclimatisation period, and there was a shift in the thermoneutral zone from 20–33 °C in summer to 15–30 °C in winter. However, no significant difference in basal metabolic rate between summer and winter was found. The results show that Rock Kestrels reduce energy expenditure at low ambient temperatures in winter as expected in an Afrotropical species.     

Seasonal variation in metabolic rate of a medium-sized frugivore, the Knysna Turaco (Tauraco corythaix)

Many seasonal thermoregulation studies have been conducted on Holarctic birds that live in predictable, highly seasonal climates with severe winters. However, relatively few studies have been conducted on their southern hemisphere Afrotropical counterparts that encounter less predictable climates with milder winters. These latter birds are expected to conserve energy in winter by downregulating their metabolic rates. Therefore in this study, metabolic rate was measured during summer and winter in Knysna Turaco, Tauraco corythaix (Musophagiformes, Musophagidae) (c. 310 g), a non-passerine, in order to test whether there is energy conservation in winter. No overall significant differences in resting metabolic rates over a range of ambient temperatures were observed between winter and summer. However, whole-organism basal metabolic rates were 18.5% higher (p=0.005) in winter than in summer (210.83±15.97 vs. 186.70±10.52 O₂ h⁻¹). Knysna Turacos had broad thermoneutral zones ranging from 20 to 28 °C in winter and 10 to 30 °C in summer. These results suggest that Knysna Turacos show seasonal thermoregulatory responses that represent cold defense rather than energy conservation, which is contrary to what was expected.     

Seasonal effects on metabolism and thermoregulation abilities of the Red-winged Starling (Onychognathus morio)

Basal metabolic rate (BMR) of birds is beginning to be viewed as a highly flexible physiological trait influenced by environmental fluctuations, and in particular changes in ambient temperatures (T_a). Southern Africa is characterized by an unpredictable environment with daily and seasonal variation. This study sought to evaluate the effects of seasonal changes in T_a on mass-specific resting metabolic rate (RMR), BMR and body temperature (T_b) of Red-winged Starlings (Onychognathus morio). They have a broad distribution, from Ethiopia to the Cape in South Africa and are medium-sized frugivorous birds. Metabolic rate (VO₂) and T_b were measured in wild caught Red-winged Starlings after a period of summer and winter acclimatization in outdoor aviaries. RMR and BMR were significantly higher in winter than summer. Body mass of Starlings was significantly higher in winter compared with summer. The increased RMR and BMR in winter indicate improved ability to cope with cold and maintenance of a high T_b. These results show that the metabolism of Red-winged Starlings are not constant, but exhibit a pronounced seasonal phenotypic flexibility with maintenance of a high T_b.     

Seasonal variation in the metabolism-temperature relation of House Sparrows (Passer domesticus) in KwaZulu-Natal,South Africa

Many birds exhibit considerable phenotypic flexibility in metabolism to maintain thermoregulation or to conserve energy. This flexibility usually includes seasonal variation in metabolic rate. Seasonal changes in physiology and behavior of birds are considered to be a part of their adaptive strategy for survival and reproductive success. House Sparrows (Passer domesticus) are small passerines from Europe that have been successfully introduced to many parts of the world, and thus may be expected to exhibit high phenotypic flexibility in metabolic rate. Mass specific Resting Metabolic Rate (RMR) and Basal Metabolic Rate (BMR) were significantly higher in winter compared with summer, although there was no significant difference between body mass in summer and winter. A similar, narrow thermal neutral zone (25–28 °C) was observed in both seasons. Winter elevation of metabolic rate in House Sparrows was presumably related to metabolic or morphological adjustments to meet the extra energy demands of cold winters. Overall, House Sparrows showed seasonal metabolic acclimatization similar to other temperate wintering passerines. The improved cold tolerance was associated with a significant increase in VO₂ in winter relative to summer. In addition, some summer birds died at 5 °C, whereas winter birds did not, further showing seasonal variation in cold tolerance. The increase in BMR of 120% in winter, compared to summer, is by far the highest recorded seasonal change so far in birds.     

Metabolic thermogenesis and evaporative water loss in the Hwamei Garrulax canorus

Basal metabolic rate (BMR) is thought to be a major hub in the network of physiological mechanisms connecting life history traits. Evaporative water loss (EWL) is a physiological indicator that is widely used to measure water relations in inter- or intraspecific studies of birds in different environments. In this study, we examined the physiological responses of summer-acclimatized Hwamei Garrulax canorus to temperature by measuring their body temperature (T_b), metabolic rate (MR) and EWL at ambient temperatures (T_a) between 5 and 40 °C. Overall, we found that mean body temperature was 42.4 °C and average minimum thermal conductance (C) was 0.15 ml O₂ g⁻¹ h⁻¹ °C⁻¹ measured between 5 and 20 °C. The thermal neutral zone (TNZ) was 31.8–35.3 °C and BMR was 181.83 ml O₂ h⁻¹. Below the lower critical temperature, MR increased linearly with decreasing T_a according to the relationship: MR (ml O₂ h⁻¹)=266.59–2.66 T_a. At T_as above the upper critical temperature, MR increased with T_a according to the relationship: MR (ml O₂ h⁻¹)=−271.26+12.85 T_a. EWL increased with T_a according to the relationship: EWL (mg H₂O h⁻¹)=−19.16+12.64 T_a and exceeded metabolic water production at T_a>14.0 °C. The high T_b and thermal conductance, low BMR, narrow TNZ, and high evaporative water production/metabolic water production (EWP/MWP) ratio in the Hwamei are consistent with the idea that this species is adapted to warm, mesic climates, where metabolic thermogenesis and water conservation are not strong selective pressures.     

Seasonal acclimation in resting metabolism of the skink, Mabuya brevicollis (Reptilia: Scincidae) from southwestern Saudi Arabia

The resting metabolic rate (RMR) of seasonally-acclimated Mabuya brevicollis of various body masses was determined at 20, 25, 30, 35 and 40 °C, using open-flow respirometry. RMR (ml g⁻¹ h⁻¹) decreased with increasing mass at each temperature. RMRs increaProd. Type: FTPsed as temperature increased. The highest and lowest Q₁₀ values were obtained for the temperature ranges 20–25 °C and 30–35 °C for the summer-acclimated lizards. The exponent of mass “b” in the metabolism-body mass relation ranged from 0.41 to 0.61. b values were lower in the autumn and winter-acclimated lizards than in spring and summer-acclimated lizards. Seasonal acclimation effects were evident at all temperatures (20–40 °C) for M. brevicollis. Winter-acclimated skinks had the lowest metabolic rates at different temperatures. The pattern of acclimation exhibited by M. brevicollis may represent a useful adaptation for lizards inhabiting subtropical deserts to promote activity during their active seasons.     

Seasonal thermoregulation in the burrowing parrot (Cyanoliseus patagonus)

Birds exposed to seasonal environments are faced with the problem of maintaining thermogenic homoeostasis. Previous studies have established that birds native to the Holarctic increase their Resting Metabolic Rate at different ambient temperatures (RMR_Ta) and Basal Metabolic Rate (BMR) in winter as an adaptation to cold temperature since winters are more severe, while their non-Holarctic counterparts generally decrease their winter BMR as an energy saving mechanism during unproductive and dry winter months. In this study, we examined seasonal thermoregulation in the burrowing parrot (Cyanoliseus patagonus), a colonial psittacine native to the Patagonian region of Argentina, a region with an unpredictable environment. We found significantly higher mass specific RMR_Ta and BMR in summer than in winter. Both summer and winter BMR of the species fell within the predicted 95% confident interval for a parrot of its size. Body mass was significantly higher in winter than in summer. The burrowing parrot had broad thermo-neutral zones in winter and summer. The circadian rhythm of core body temperature (T_b) of burrowing parrots was not affected by season, showing that this species regulated its T_b irrespective of season. These results suggest that the burrowing parrots' seasonal thermoregulatory responses represent that of energy conservation which is important in an unpredictable environment.     

Effects of short-term acclimation on thermoregulatory responses of the rock kestrel, Falco rupicolus

The effects of a short-term acclimation period on basal metabolic rate (BMR) and resting metabolic rate (RMR) were measured in captive-bred Rock Kestrels (Falco rupicolus). Birds were exposed to winter conditions (pre-acclimation) in a semi-natural environment before they were acclimated for a period of 3 weeks at a constant temperature of 25 °C and a constant light:dark cycle (12:12 h) (post-acclimation). After acclimation the kestrels showed changes in RMR, BMR and the width of the thermoneutral zone. There was inter- and intra-individual phenotypic plasticity in BMR and RMR both pre- and post-acclimation. However, more inter-individual variation was seen after acclimation. This study concurs with recent suggestions that phenotypic plasticity in BMR is prevalent in avian physiology, and thus a single-species-specific BMR value may not be representative. Furthermore, comparative avian studies of BMR need to account for phenotypic plasticity.     

Seasonal effects on thermoregulatory abilities of the Wahlberg's epauletted fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal,South Africa

Seasonal variations in ambient temperature (T_a) require changes in thermoregulatory responses of endotherms. These responses vary according to several factors including taxon and energy constraints. Despite a plethora of studies on chiropteran variations in thermoregulation, few have examined African species. In this study, we used the Wahlberg's epauletted fruit bat (Epomophorus wahlbergi, body mass≈115 g) to determine how the thermoregulatory abilities of an Afrotropical chiropteran respond to seasonal changes in T_a. Mass specific Resting Metabolic Rates (RMR_Ta) and basal metabolic rate (BMR) were significantly higher in winter than in summer. Furthermore, winter body mass was significantly higher than summer body mass. A broad thermoneutral zone (TNZ) was observed in winter (15–35 °C) compared with summer (25–30 °C). This species exhibited heterothermy (rectal and core body temperature) during the photophase (bats' rest-phase) particularly at lower T_as and had a low tolerance of high T_as. Overall, there was a significant seasonal variation in the thermoregulatory abilities of E. wahlbergi. The relative paucity of data relating to the seasonal thermoregulatory abilities of Afrotropical bats suggest further work is needed for comparison and possible effects of climate change, particularly extreme hot days.     

Continuous growth through winter correlates with increased resting metabolic rate but does not affect daily energy budgets due to torpor use

Small mammals that are specialists in homeothermic thermoregulation reduce their self-maintenance costs of normothermy to survive the winter. By contrast, heterothermic ones that are considered generalists in thermoregulation can lower energy expenditure by entering torpor. It is well known that different species vary the use of their strategies to cope with harsh winters in temperate zones; however, little is still known about the intraspecific variation within populations and the associated external and internal factors. We hypothesized that yellow-necked mice Apodemus flavicollis decrease their resting metabolic rate (RMR) from autumn to winter, and then increase it during spring. However, since the alternative for seasonal reduction of RMR could be the development of heterothermy, we also considered the use of this strategy. We measured body mass (m_b), RMR, and body temperature (T_b) of mice during 2 consecutive years. In the 1st year, mice decreased whole animal RMR in winter, but did not do so in the 2nd year. All mice entered torpor during the 2nd winter, whereas only a few did so during the first one. Mice showed a continuous increase of m_b, which was steepest during the 2nd year. The relationship between RMR and m_b varied among seasons and years most likely due to different mouse development stages. The m_b gain at the individual level was correlated positively with RMR and heterothermy. This indicates that high metabolism in winter supports the growth of smaller animals, which use torpor as a compensatory mechanism. Isotope composition of mice hair suggests that in the 1st year they fed mainly on seeds, while in the 2nd, they likely consumed significant amounts of less digestible herbs. The study suggests that the use of specialist or generalist thermoregulatory strategies can differ with environmental variation and associated differences in developmental processes.     

The use of small subcutaneous transponders for quantifying thermal biology and torpor in small mammals

Remote measurements of body temperature (T_b) in animals require implantation of relatively large temperature-sensitive radio-transmitters or data loggers, whereas rectal temperature (T_rec) measurements require handling and therefore may bias the results. We investigated whether ∼0.1 g temperature-sensitive subcutaneously implanted transponders can be reliably used to quantify thermal biology and torpor use in small mammals. We examined (i) the precision of transponder readings as a function of temperature and (ii) whether subcutaneous transponders can be used to remotely record subcutaneous temperature (T_sub). Five adult male dunnarts (Sminthopsis macroura, body mass 24 g) were implanted with subcutaneous transponders to determine T_sub as a function of time and ambient temperature (T_a), and in comparison to thermocouple readings of T_rec. Transponder temperature was highly correlated with water bath temperature (r²=0.96–0.99) over a range of approximately 10.0–40.0 °C. Transponders provided reliable data (±0.6 °C) over the T_sub of 21.4–36.9 °C and could be read from a distance of up to 5 cm. Below 21.4 °C, accuracy was reduced to ±2.8 °C, but individual transponder accuracy varied. Consequently, small subcutaneous transponders are useful to remotely quantify thermal physiology and torpor patterns without having to disturb the animal and disrupt torpor. Even at T_sub<21.4 °C where the accuracy of the temperature readings was reduced, transponders do provide reliable data on whether and when torpor is used.     

Seasonal effects on the thermoregulation of invasive rose-ringed parakeets (Psittacula krameri)

Invasive species are a major threat to global biodiversity. Rose-ringed parakeets Psittacula krameri are widely established outside their native range and are successful invaders in many countries, including South Africa. Physiological and behavioral responses to environmental conditions are considered to be major factors that influence the abundance and distribution of birds. As rose-ringed parakeets are able to tolerate wide varieties of climatic conditions as invaders, it is important to understand their physiological responses to these. This study examined the effects of seasonal changes in ambient temperatures (T_a) on metabolic rate and body temperature (T_b) of captive-bred rose-ringed parakeets. Resting metabolic rate at various T_a and basal metabolic rate were significantly lower in winter compared to summer, and the thermo-neutral zone was broader in winter than in summer. There was no significant difference in body mass (M_b) between seasons. These parakeets showed seasonal thermoregulatory responses that represented energy conservation as expected, rather than cold tolerance. They were relatively tolerant of low T_a and showed no hypothermia at 5 °C. Our results suggest that this species is physiologically and behaviorally equipped to cope with a range of climatic situations and this partly explains their global success as an invader species.     

Body temperature variation of South African antelopes in two climatically contrasting environments

To understand the adaptive capacity of a species in response to rapid habitat destruction and climate change, we investigated variation in body temperature (T_b) of three species of antelope, namely eland, blue wildebeest and impala, using abdominally-implanted temperature data loggers. The study was conducted at two climatically contrasting environments in South Africa, one with a less seasonal and mild winter (Mapungubwe National Park) and the other with a more seasonal, long and cold winter (Asante Sana Game Reserve). Since the habitat with long and cold winters would be suboptimal for these African antelopes, which evolved in less seasonal and hot environments, antelopes in Asante Sana were expected to exhibit a larger amplitude in T_b and a lower minimum body temperature (Min T_b) during winter to reduce T_b and the ambient temperature (T_b−T_a) gradient to save energy. In both eland and impala, 24-h body temperature amplitude did not differ between the study sites, regardless of season. Conversely, wildebeest in Mapungubwe showed a higher variability in the 24-h amplitude of body temperature and also a lower Min T_b during winter and spring than the wildebeest in Asante Sana. This variation in T_b among Mapungubwe wildebeest was influenced by both the amplitude of ambient temperature (positive) and cumulative rainfall (negative), which was not the case for wildebeest in Asante Sana. We propose that the low Min T_b of wildebeest in Mapungubwe was the result of nutritional stress during winter and spring; an evident response even during a year of average rainfall. Therefore, these wildebeest apparently live in a physiologically stressful environment. With the predicted increase in the frequency and intensity of drought periods in southern Africa, wildebeest and other grazers, will likely experience greater nutritional stress in the future.     

Body temperature patterns in two syntopic elephant shrew species during winter

We measured body temperature (T_b) in free-ranging individuals of two species of elephant shrews, namely western rock elephant shrews (Elephantulus rupestris) and Cape rock elephant shrews (E. edwardii), during winter in a winter-rainfall region of western South Africa. These syntopic species have similar ecologies and morphologies and thus potential for large overlaps in diet and habitat use. Unexpectedly, they displayed different T_b patterns. Western rock elephant shrews were heterothermic, with all individuals decreasing T_b below 30 °C on at least 34% of nights. The level of heterothermy expressed was similar to other species traditionally defined as daily heterotherms and was inversely related to T_a, as is commonly seen in small heterothermic endotherms. In contrast, Cape rock elephant shrews rarely allowed their T_b to decrease below 30 °C. The level of heterothermy was similar to species traditionally defined as homeotherms and there was no relationship between the level of heterothermy expressed and T_a. In both species, the minimum daily T_b was recorded almost exclusively at night, often shortly before sunrise, although in some individuals minimum T_b occasionally occurred during the day. The interspecific variation in T_b patterns among Elephantulus species recorded to date reiterates the importance of ecological determinants of heterothermy that interact with factors such as body mass and phylogeny.     

Respiration rate and oxy-regulatory capacity in cold stenothermal chironomids

The effects of temperature and oxygen saturation on the respiration rate of two cold stenothermal chironomids, Diamesa insignipes and Pseudodiamesa branickii were investigated. Fourth instar larvae were collected in winter in a glacio-rhithral stream (1300 m a.s.l., Alps, NE-Italy) and their respiration rate was measured with a Clark's electrode in the range 0-14 °C. The respiration rate was significantly higher in D. insignipes than in P. branickii at low temperatures (≤4 °C), higher in P. branickii between 8 and 12 °C and comparable at 14 °C. Higher values of R (regulation value), R_25% (respiration rate at 25% oxygen saturation) and b₁/b₂ (slope ratio in piecewise linear regression), and lower values of P_c (critical pressure) and I (initial decrease) were recorded in P. branickii than in D. insignipes. These values are compatible with oxy-regulatory behaviour in P. branickii, whereas D. insignipes appeared to be almost an oxy-conformer. On the basis of this autoecological information, new implications regarding survival of species from cold, high altitude habitats under changing climatic conditions are made.     

Seasonal variation on metabolism and thermoregulation in Chinese bulbul

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Seasonal changes in a bird's physiology and behavior are considered to be a part of an adaptive strategy for survival and reproductive success. To understand modes of metabolic adaptations, the metabolic rate (Vo₂), body temperature (T_b), and thermal conductance (C) of the Chinese bulbul (Pycnonotus sinensis) in the Zhejiang Province of China were determined in the summer and the winter at a temperature range from 5 to 35 °C, respectively.     

Metabolic responses of sand fiddler crabs, Uca pugilator, in northwest Florida to seasonal temperature change

Metabolic responses of sand fiddler crab, Uca pugilator, populations in northwest Florida are greatly influenced by seasonal temperature fluctuations. Crabs acclimated at 20 °C and immediately transferred to either 14 or 26 °C produced an acute metabolic response with respective temperature quotient (Q₁₀) values of 3.46 and 3.91. Crabs acclimated at 10 and 20 °C exhibited a Q₁₀ of 2.62 indicating a partial compensation response. A brumation (reverse) response (Q₁₀ value of 20.11) was observed for acclimated crabs between 5 and 10 °C. Brumation is advantageous during winter when food supplies are scarce and crabs must survive extensive periods of inactivity.     

Acclimation of the intertidal red alga Bangiopsis subsimplex (Stylonematophyceae) to salinity changes

The effect of salinity on growth, photosynthetic performance and osmotic acclimation was investigated in the eulittoral red algal species Bangiopsis subsimplex (Stylonematophyceae). The strain grew in a broad salinity range between 1 and 70 psu showing optimum growth between 10 and 50 psu. The saturation point I_k of the photosynthesis irradiance curves ranged between 153 and 83 μmol photons m^− 2 s^− 1 at all salinities and indicates an adaptation of B. subsimplex to moderate radiation conditions. Adjustments on the photosynthetic level (non-photochemical quenching) were sufficient to prevent damage to the photosynthetic apparatus as F_v/F_m values were constantly high (> 0.7) even when grown at the most hypo- and hypersaline conditions. As main low molecular weight carbohydrates, B. subsimplex contains the heteroside digeneaside and the polyol sorbitol. Digeneaside concentration was low and almost unchanged after hypersaline treatment (< 20 μmol g^− 1 DW), i.e. it did not play a role in osmotic acclimation. By contrast, sorbitol levels increased linearly from 150 to 380 μmol g^− 1 DW with increasing salinities between 5 and 60 psu, indicating its important function as an osmolyte and compatible solute under hypersaline conditions. The data presented are consistent with the natural habitat of B. subsimplex, i.e. the upper eulittoral zone.     

Seasonal changes in body mass and thermogenesis in tree shrews (Tupaia belangeri): The roles of photoperiod and cold

Environmental factors play an important role in the seasonal adaptation of body mass and thermogenesis in small, wild mammals. To determine the contributions of photoperiod and cold on seasonal changes in energy metabolism and body mass, the resting metabolic rates (RMR), nonshivering thermogenesis (NST), energy intake and gut morphology of the tree shrews were determined in winter and summer and in laboratory acclimated animals. Body mass, RMR and NST increased in winter, and these changes were mimicked by exposing animals to short-day photoperiod or cold in the animal house. Energy intake and digested energy also increased significantly in winter, and also during exposure of housed animals to both short-day photoperiod and cold. The lengths and weights of small intestine increased in winter. These results indicated that Tupaia belangeri overcomes winter thermoregulatory challenges by increasing energy intake and thermogenesis, and adjusted gut morphology to balance the total energy requirements. Short-day photoperiod and cold can serve as environmental cues during seasonal acclimatization.     

Field-acclimated Gossypium hirsutum cultivars exhibit genotypic and seasonal differences in photosystem II thermostability

Previous investigations have demonstrated that photosystem II (PSII) thermostability acclimates to prior exposure to heat and drought, but contrasting results have been reported for cotton (Gossypium hirsutum). We hypothesized that PSII thermotolerance in G. hirsutum would acclimate to environmental conditions during the growing season and that there would be differences in PSII thermotolerance between commercially-available U.S. cultivars. To this end, three cotton cultivars were grown under dryland conditions in Tifton Georgia, and two under irrigated conditions in Marianna Arkansas. At Tifton, measurements included PSII thermotolerance (T₁₅, the temperature causing a 15% decline in maximum quantum yield), leaf temperatures, air temperatures, midday (1200 to 1400 h) leaf water potentials (Ψ_MD), leaf-air vapor pressure deficit (VPD), actual quantum yield (Φ_PSII) and electron transport rate through PSII (ETR) on three sample dates. At Marianna, T₁₅ was measured on two sample dates. Optimal air and leaf temperatures were observed on all sample dates in Tifton, but PSII thermotolerance increased with water deficit conditions (Ψ_MD = −3.1 MPa), and ETR was either unaffected or increased under water-stress. Additionally, T₁₅ for PHY 499 was ∼5 °C higher than for the other cultivars examined (DP 0912 and DP 1050). The Marianna site experienced more extreme high temperature conditions (20–30 days T_max ≥ 35 °C), and showed an increase in T₁₅ with higher average T_max. When average T₁₅ values for each location and sample date were plotted versus average daily T_max, strong, positive relationships (r² from .954 to .714) were observed between T_max and T₁₅. For all locations T₁₅ was substantially higher than actual field temperature conditions. We conclude that PSII thermostability in G. hirsutum acclimates to pre-existing environmental conditions; PSII is extremely tolerant to high temperature and water-deficit stress; and differences in PSII thermotolerance exist between commercially-available cultivars.