Conquering the night: understanding nocturnal migration in birds

Abstract

Migration is a biologically distinct and unique phenomenon that enables the birds to migrate twice-a-year between the breeding and wintering grounds. These movements are known as spring and autumn migration, respectively. Depending on their inherent programming, the migratory birds may fly during day or night or both. Different environmental factors such as, temperature, food, predator pressure and physiological demands of energy storage and expenditure, contribute to the pattern of migrations, day or nighttime. Since, most of them are nighttime migrants they have to make dramatic changes in their physiology and behavior to transform them from being diurnal to predominantly nocturnal. These changes result in different life history stages (LHSs) such as migration, reproduction and molt, in their annual cycle, which are regulated by endogenous circadian and circannual clocks. As a result, the birds start preparing well in advance for the approaching LHS. The present review focuses on behavioral strategies of a nocturnal migrant and understanding of the possible physiological responses to ensure successful migration.     

Even a mild spell of cold weather affects feeding in migrating redheaded buntings

We investigated whether a climatic change in temperature affected daily food intake in migrating male redheaded buntings. Groups of adult male birds (n = 18) were photoinduced into migratory phenotype under increasing spring daylengths (NDL); as the birds began to exhibit night restlessness, Zugunruhe, these were allocated into groups, either with ambient (NDL, variable daily temperature: maximum – 29–44 °C and minimum – 16–33 °C; for food intake (six birds) and activity recording, six birds) until 2 weeks after they concluded migration or with constant temperature (NDT, 22 ± 1 °C; for food intake (six birds)) conditions. As day length increased March onwards, daily food intake increased (hyperphagia) in NDL and NDT groups. However, hyperphagia was slower in NDT birds as compared to NDL birds, suggesting that altered ambient temperature affects daily food intake in migrating buntings. Another group of 12 birds were held under constant daylengths (12L:12D; EDT and constant temperature 22 ± 1 °C). Although the onset of Zugunruhe was delayed under EDT, the day of onset of Zugunruhe was taken as day 0. Daily food intake and body weight before and during migration of EDT birds were compared with that of NDT and NDL groups. Daily food intake and body weight increased in all migrating birds, but hyperphagia continued post-migration in NDT birds. The study suggests that constantly suboptimal temperature despite increasing daylength, NDT, appeared to affect feeding and body weight of migratory buntings as evident from continued hyperphagia and body weight gain, even after concluding migrating activity.     

Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon)

Background

In many birds, day length (=photoperiod) regulates reproductive cycle. The photoperiodic environment varies between different seasons and latitudes. As a consequence, species at different latitudes may have evolved separate photoperiodic strategies or modified them as per their adaptive need. We studied this using house sparrow as a model since it is found worldwide and is widely investigated. In particular, we examined whether photoperiodism in house sparrows (Passer domesticus) at 27°N, 81°E shared features with those exhibited by its conspecifics at high latitudes.

Results

Initial experiment described in the wild and captive conditions the gonad development and molt (only in captives) cycles over a 12-month period. Both male and female sparrows had similar seasonal cycles, linked with annual variations in day length; this suggested that seasonal reproduction in house sparrows was under the photoperiodic control. However, a slower testis and attenuated follicular growth among captives indicated that other (supplementary) factors are also involved in controlling the reproductive cycle. Next experiment examined if sparrows underwent seasonal variations in their response to stimulatory effects of long day lengths. When birds were transferred every month over a period of 1 year to 16 hours light:8 hours darkness (16L:8D) for 17–26 weeks, there was indeed a time-of-year effect on the growth-regression cycle of gonads. The final experiment investigated response of house sparrows to a variety of light-dark (LD) cycles. In the first set, sparrows were exposed for 31 weeks to photoperiods that were close to what they receive in between the period from sunrise to sunset at this latitude: 9L:15D (close to shortest day length in December), 12L:12D (equinox, in March and September) 15L:9D (close to longest day length in June). They underwent testicular growth and regression and molt in 12L and 15L photoperiods, but not in 9L photoperiod. In the second set, sparrows were exposed for 17 weeks to photoperiods with light periods extending to different duration of the daily photosensitivity rhythm (e.g. 2L:22D, 6L:18D, 10L:14D, 14L:10D, 18L:6D and 22L:2D). Interestingly, a slow and small testicular response occurred under 2L and 10L photoperiods; 6L:18D was non-inductive. On the other hand, 14L, 18L and 22L photoperiods produced testicular growth and subsequent regression response as is typical of a long day photostimulation.

Conclusion

Subtropical house sparrows exhibit photoperiodic responses similar to that is reported for its population living at high latitudes. This may suggest the conservation of the photoperiodic control mechanisms in birds evolved over a long period of time, as a physiological strategy in a temporally changing environment ensuring reproduction at the best suited time of the year.     

Neural Correlates of Migration: Activation of Hypothalamic Clock(s) in and out of Migratory State in the Blackheaded Bunting (Emberiza melanocephala)

Background

Many vertebrates distinguish between short and long day lengths using suprachiasmatic nuclei (SCN). In birds particular, the mediobasal hypothalamus (MBH) is suggested to be involved in the timing of seasonal reproduction. This study investigated the response of SCN and MBH to a single long day, and the role of MBH in induction of the migratory phenotype in night-migratory blackheaded buntings.

Methodology/Principal Findings

Experiment 1 immunocytochemically measured c-fos in the SCN, and c-fos, vasoactive intestinal peptide (VIP) and neuropeptide Y (NPY) in the MBH of buntings exposed to a 20 h light period. Long light period induced significantly stronger c-fos expression, measured as number of c-fos-like immunoreactive (c-fos-lir) cells, in MBH, but not in the SCN. Within the MBH, c-fos-lir cells were significantly denser in the inferior hypothalamic nucleus (IH) and infundibular nucleus (IN), but not in the dorsomedial hypothalamus (DMH). IH and IN also had significantly increased number of VIP and NPY labeled cells. DMH had significantly increased number of VIP labeled cells only. Experiment 2 assayed c-fos, VIP and NPY immunoreactivities in the middle of day and night in the MBH of buntings, after seven long days (day active, non-migratory state) and after seven days of Zugunruhe (night active, migratory state) in long days. In the migratory state, the number of c-fos-lir cells was significantly greater only in DMH; VIP-lir cells were denser in all three MBH regions suggesting enhanced light sensitivity at night. The denser NPY-lir cells only in IN in the non-migratory state were probably due to premigratory hyperphagia.

Conclusions/Significance

In buntings, SCN may not be involved in the photoperiod-induced seasonal responses. MBH contains the seasonal clock sensitive to day length. VIP and NPY are parts of the neuroendocrine mechanism(s) involved, respectively, in sensing and translating the photoperiodic message in a seasonal response.     

Altered light conditions during spring: effects on timing of migration and reproduction in migratory redheaded bunting (Emberiza bruniceps)

Photoperiod is the most consistent environmental cue, and therefore, any change in anticipated light environment may affect subsequent response under long days. To test this hypothesis, photosensitive migratory redheaded buntings (Emberiza bruniceps) were exposed to altered photoperiods for 4 weeks [short days (SP, 8L:16D, group 1; control), short days alternated with constant dim light (SP/LL_dim; group 2), constant dim light (LL_dim; group 3) and constant bright light (LL_bright; group 4)] before being transferred to long days (LP; 16L:8D) for 15 weeks. Group differences in long-day-induced responses were observed. The onset of migratory restlessness (Zugunruhe) was earliest in LL_bright but persisted for maximum period in LL_dim group. The LL_dim group attained peak testis size significantly delayed and had more food consumption under long days. The results suggest that the altered photoperiodic exposure during photosensitive stage affects the seasonal phenotypes such as migration and reproduction in migratory buntings.     

Daily levels and rhythm in circulating corticosterone and insulin are altered with photostimulated seasonal states in night-migratory blackheaded buntings

The circadian rhythms are involved in the photostimulation of seasonal responses in migratory blackheaded buntings. Here, we investigated whether changes in daily levels and rhythm in corticosterone (cort) and insulin secretions were associated with transitions in the photoperiodic seasonal states. Buntings were exposed to short days to maintain the winter (photosensitive) non-migratory state, and to long days for varying durations to induce the premigratory, migratory (shown by migratory restlessness at night, Zugunruhe) and summer non-migratory (photorefractory) states. We monitored activity patterns, and measured plasma cort and insulin levels at six and four times, respectively, over 24 h in each seasonal state. Buntings were fattened and weighed heavier, and exhibited intense nighttime activity in the migratory state. The daytime activity patterns also showed seasonal differences, with a bimodal pattern with morning and evening activity bouts only in the summer non-migratory state. Further, the average baseline hormone levels were significantly higher in premigratory and migratory than in the winter non-migratory state. Both cort and insulin levels showed a significant daily rhythm, but with seasonal differences. Whereas, cort rhythm acrophases (estimated time of peak secretion over 24 h) were at night in the winter non-migratory, premigratory and migratory states, the insulin rhythm acrophases were found early in the day and night in winter and summer non-migratory states, respectively. These results suggest that changes in daily levels and rhythm in cort and insulin mediate changes in the physiology and behavior with photostimulated transition in seasonal states in migratory blackheaded buntings.     

Investigations of photoperiodically induced fattening in migratory blackheaded bunting (Emberiza melanocephala)(Ayes)

The body fattening and weight gain preceding vernal migration in birds is timed by a set of environmental factors of which daylength is predominant. However, the mechanism(s) by which these events is determined is poorly understood. Previous investigations on a photoperiodic migratory species, the blackheaded bunting ( Emberiza melanocephala ), indicate the involvement of a light-sensitive circadian rhythm during initiation of fat deposition and body weight gain. This communication presents data from another set of experiments aimed to characterize further the mechanism(s) of fat deposition in the same species.
Groups of photosensitive, unstimulated and stimulated birds were subjected to transfer and superimposition experiments for 30 days. While the former set included shifting of long-day (LD) birds to DD, SD (short days), DD/LD and SD/LD, in the latter a 90-minute bright light was superimposed at two different times of the day during the dim-green lighted phase 15L:9D of varying intensity. Birds were weighed at the beginning and at the end of experiments. Those in transfer cycles were also weighed at 10-day intervals. The results suggest that the premigratory body fattening and weight gain in blackheaded buntings is light dependent and timed by environmental daylength in accordance with the photosensitive endogenous circadian rhythm (ECR). They also show that the photoperiodic responses in birds in general are mediated by circadian rhythm(s).     

Involvement of threshold photoperiod in control of reproductive rhythmicity in migratory blackheaded bunting, Emberiza melanocephala

To explore the need for minimum threshold photoperiodicity in regulation of metabolic and reproductive activities of a migratory finch, various programmed light-dark (LD) schedules, such as P1 (3L/21D), P2 (6L/18D), P3 (9L/15D), P4 (12L/12D), P5 (15L/9D), P6 (18L/6D), P7 (21L/3D), and P8 (24L/0D), have been used on photosensitive female blackheaded buntings for 42 days. Results indicate that the photoperiodic thresholds of 3 h, 6 h, and 9 h completely failed to have any response on buntings, while threshold photoperiodicities of 12 h, 15 h, 18 h, 21 h, and 24 h had significant effect (P < .001) on body weight, ovarian weight, and circulating plasma estradiol concentration, suggesting the role of the photoperiod as a primary environmental source to regulate various metabolic and reproductive functions. Further, it has been suggested that the threshold photoperiod in this species appears to be of 12 h duration.     

长白山北坡鹀属鸟类群落结构的研究

鹀属(Emberiza Linnaeus)鸟类种类繁多,仅我国就有26种(郑作新,1973),它们分布广泛,数量较多,几乎遍布全国各地。这些鸟类和人们的经济关系较为密切。有关它们和农业方面的关系已有过报道(贾相刚等,1973)。但是,和森林的关系,资料并不多。 关于鸟类群落的研究,对鸟类生态学的进一步发展有很重要的意义。这方面的工作,国     

Daily light regulates seasonal responses in the migratory male redheaded bunting (Emberiza bruniceps)

This study analyzed the role of day length in regulation of seasonal body fattening and testicular growth in a latitudinal Palaearctic-Indian migrant, the redheaded bunting (Emberiza bruniceps). When exposed to increasing photoperiods (hours of light: hours of darkness; 11.5L:12.5D, 12L:12D, 12.5L:11.5D, 13L:11D, 14L:10D, and 18L:6D) for 9-12 weeks, buntings responded in a photoperiod-dependent manner and underwent growth and regression cycle under photoperiods of > or =12 hr per day. Also, the response to a long photoperiod of birds that were held under natural photoperiods at 27 degrees N for 2 years was similar to those who arrived the same year from their breeding grounds ( approximately 40 degrees N), suggesting that the experience of higher amplitude day-night (light-dark, LD) cycles during migratory and breeding seasons were not critical for the subsequent response (initiation-termination-reinitiation) cycle. Another experiment examined entrainment of the circadian photoperiodic rhythm in buntings by subjecting them to T=24+/-2 hr LD-cycles with 8 hr photophase and to T=22 and 24 hr with 11 hr photophase. The results showed a reduction in critical day length under T=22 hr LD-cycle. In the last experiment, we constructed an action spectrum for photoperiodic induction by exposing birds for 4.5 weeks to 13L:11D of white (control), blue (450 nm), or red (640 nm) light at irradiances ranging from 0.028 to 1.4 W m(-2). The threshold light irradiance for photoinduction was about 10-fold higher for blue light, than for red and white lights. These results conclude that the daily light of the environment regulates the endogenous program that times seasonal responses in body fattening and testicular cycles of the redheaded bunting.     

Seasonal survival estimation for a long-distance migratory bird and the influence of winter precipitation

Conservation of migratory animals requires information about seasonal survival rates. Identifying factors that limit populations, and the portions of the annual cycle in which they occur, are critical for recognizing and reducing potential threats. However, such data are lacking for virtually all migratory taxa. We investigated patterns and environmental correlates of annual, oversummer, overwinter, and migratory survival for adult male Kirtland’s warblers (Setophaga kirtlandii), an endangered, long-distance migratory songbird. We used Cormack–Jolly–Seber models to analyze two mark–recapture datasets: 2006–2011 on Michigan breeding grounds, and 2003–2010 on Bahamian wintering grounds. The mean annual survival probability was 0.58 ± 0.12 SE. Monthly survival probabilities during the summer and winter stationary periods were relatively high (0.963 ± 0.005 SE and 0.977 ± 0.002 SE, respectively). Monthly survival probability during migratory periods was substantially lower (0.879 ± 0.05 SE), accounting for ~44% of all annual mortality. March rainfall in the Bahamas was the best-supported predictor of annual survival probability and was positively correlated with apparent annual survival in the subsequent year, suggesting that the effects of winter precipitation carried over to influence survival probability of individuals in later seasons. Projection modeling revealed that a decrease in Bahamas March rainfall >12.4% from its current mean could result in negative population growth in this species. Collectively, our results suggest that increased drought during the non-breeding season, which is predicted to occur under multiple climate change scenarios, could have important consequences on the annual survival and population growth rate of Kirtland’s warbler and other Neotropical–Nearctic migratory bird species.     

Environmental and hormonal control of vernal migration in redheaded bunting (Emberiza bruniceps)

This paper reviews the factors and mechanisms which result in the development of the metabolic state characteristic of migration with special reference to a palaeotropic migrant the redheaded bunting,Emberiza bruniceps. Changes in climatic conditions and food supply act as proximate triggers of migratory behaviour in partial migrants. Typical migrants like buntings use daylength as a cue but the exact mechanism of how photoperiodic information is translated in terms of migratory events is still not known. Almost entirely the photoperiodic effects have been explained on the basis of the involvement of hypothalamo/hypophyseal system. We feel mechanism(s) other than those acting through neuroendocrine system may be equally important. Furthermore the role of temperature has not been adequately explored so far. Our observations indicate the possibility that redheaded buntings might integrate the information received from photoperiod with environmental temperature (and other factors?) resulting in the development of migratory state. The physiological control of avian migration is much less understood. Majority of papers have centered around the ‘gonadal hypothesis’ of Rowan supporting or contradicting it without providing conclusive evidence. Pituitary prolactin has also been shown to be implicated although the mechanism of action is only speculative. Conclusive evidence for the involvement of thyroid hormones (thyroxine, T4; triiodothyronine, T3) in the physiological timing of migration has been produced attributing independent roles to T4 and T3. It is suggested that seasonal variation in peripheral conversion of T4 to T3 could serve as an effective strategy to render available the required thyroid hormones T4 and/or T3 during different phases of the year thus accounting for the metabolic switch over from T4-dependent moult to T3-dependent migratory fat deposition and zugunruhe and also ensuring preclusion of simultaneous occurrence of these mutually incompatible events. Considering that the number of environmental and physiological factors influence this mechanism and considering that thyroid hormone molecule has been put to a wide range of usage during the course of evolution the mechanism(s) of peripheral conversion of T4-T3 may assume great flexibility and have selective value-especially in migration which is known to have evolved several times in diverse avian families. The attractiveness of this hypothesis lies in the fact that it has potential to explain the both physiological development of the metabolic state of migration and at the same time the physiological timing of migration not only with respect to the cycle of environment but also with respect to other conflicting seasonal events (moult and reproduction).     

Diversification at high latitudes: speciation of buntings in the genus Plectrophenax inferred from mitochondrial and nuclear markers

High‐latitude diversification is a process characterized by speciation and extinction due to climatically driven vicariance and dispersal events. McKay’s buntings (Plectrophenax hyperboreus) are high‐latitude island endemic songbirds, and their global range is restricted to Beringia. Snow buntings (P. nivalis), their closest relatives, are distributed throughout the Holarctic, breeding in available habitat surrounding the island range of McKay’s buntings. We sequenced 1123 base pairs of mitochondrial DNA for 40 individuals of each species and analysed a total of 913 AFLPs for 57 individuals. Both marker types suggested weak but significant genetic differentiation. Analysis of sequence data indicated divergence occurring when the current breeding range of McKay’s buntings was a hill on the Beringian steppe (～18 400 to ～73 700 years before present), suggesting that snow buntings were restricted to lower latitudes by ice sheets. Ancestral effective population size estimates indicate a founder event in McKay’s buntings followed by an expansion and then a reduction in effective size. Rising sea levels and asymmetric hybridization from McKay’s buntings into the postglacially‐colonizing population of snow buntings could account for this reduction. Reproductive isolation is likely maintained through differential arrival dates on breeding grounds and the high breeding density of McKay’s buntings. This recent, high‐latitude divergence best fits a model of founder event speciation driven by vicariance and oscillations in habitat due to climate change.     

Diapause termination in two species of damselflies

Larvae of two species of damselflies, Enallagma hageni and E. aspersum, were collected in southwestern North Carolina and subjected to different combinations of daylength (SD, 11 hr day; LD, 14 hr day) and temperature to determine the factor critical in the termination of diapause. Diapausing larvae were collected in September, and 15 comparable groups of each species were given pretreatments (SD, 10°C; LD, 10°C; or SD, 21°C) for 2, 4, or 8 weeks and then transferred to SD, 21°C or LD, 21°C until emergence. Control groups were maintained under both photoperiods at 21°C.Response times (days from collection to emergence) for both species showed that rapid development required transfer to LD, 21°C regardless of the type of pretreatment or length of exposure. Larvae transferred to LD, 21°C after exposure to any of the three types of pretreatment for equal lengths of time developed at similar rates. Pretreatments at 10°C, which were equally effective with SD or LD, stimulated subsequent rapid development at LD, 21°C to a greater extent than continuous exposure to LD, 21°C conditions, and the longer the exposure to 10°C, the faster the subsequent response. Pretreatments at SD, 21°C also resulted in rapid development, similar to that of larvae exposed to 10°C, upon transfer to LD, 21°C conditions. Long daylengths administered only during pretreatments did not effect rapid development, since all larvae responded slowly when transferred to SD, 21°C. Diapause termination, therefore, was effected by LD, 21°C conditions preceded by exposure to either low temperatures, during which the photoperiod was not important, or short daylengths at 21°C.     

Northward expansion and climatic factors affecting the distribution limits of Cheilomenes sexmaculata (Coleoptera: Coccinellidae) in Japan

The distributional expansion of the ladybird beetle Cheilomenes sexmaculata (Fabricius) in Japan was analyzed based on literature surveys and observations of 1,312 individual specimens collected from 1918 to 2005. An expansion toward higher latitudes, from Kyushu (33°N) to central Honshu (36°N), was observed between 1910 and the early 1990s. Multiple regression analysis showed that the presence of this beetle was associated with an annual mean temperature but not with the mean minimum temperature in the coldest month, and 95 % occurrence probability of this beetle was obtained in a locality at 15.1 °C annual mean temperature. The northward expansion of this species synchronizes with increasing areas where an annual mean temperature is more than 15 °C. Therefore, climatic warming over the past 100 years is considered as a major factor influencing the northward expansion of this species.     

Metabolic response to changes in temperature in northern wheatears from an arctic and a temperate populations

Until recently it had been widely accepted that birds are energetically adapted to the latitude they inhabit, having an increased basal metabolic rate (BMR) at higher latitudes. Latterly, this general view has been questioned and the influence of phenotypic flexibility, due to factors such as habitat, life‐history or acclimatization has received increased attention. In particular, focus has been directed towards comparing species from arid and mesic habitats, but less attention has been given to species which breed in cold climates. We chose to study northern wheatears Oenanthe oenanthe from two populations at different latitudes (southern Norway, Iceland), but with similar life‐histories and habitat requirements throughout the year, in a common‐garden experiment. In order to assess true latitudinal trends in metabolic rate, we estimated the nocturnal resting metabolic rate (RMR) of northern wheatears from southern Norway and Iceland at different temperatures from 0° to 30°C. We found that Norwegian birds had overall lower metabolic rates than Icelandic birds, which were also slightly larger. This difference was not observed at 0°C, which might indicate that Icelandic birds might rely on better feather insulation reducing metabolic costs at very low temperatures. At temperatures above 10°C birds of both populations had constant metabolic values, indicating that their thermoneutral range almost completely covered the temperatures experienced during the breeding period. This study shows that the northern wheatear, which is one of only a few insectivorous long‐distance migratory songbirds occurring at such high latitudes, has evolved metabolic adaptations to life at cold temperatures which are endogenously determined.     

Biochronometry of photoperiodically induced fat deposition in a migratory finch, the Blackheaded bunting (Emberiza melanocephala) (Aves)

This investigation attempts to identify the mechanism(s) involved in the fat deposition in a photoperiodic migratory species, the Blackheaded bunting ( Emberiza melanocephala ). Groups of photosensitive male buntings were exposed to resonance, interrupted night, and ultra-short-day light cycles for 35, 42 and 75 days, respectively. Birds were weighed at the beginning and at the end of the experiments. Those exposed to ultra-short-day light cycles were also weighed at critical intervals during the treatment period. Our results indicate that: (a) a light-sensitive rhythm with a period of about 24 hr is involved in the photoperiodic induction of premigratory fattening and weight gain in Blackheaded buntings: (b) buntings possess a bimodal pattern 'of sensitivity to photoperiods that induce fattening, and (c) this endogenous circadian rhythm can be entrained by an ultrashort photophase of 3 h if the latter is coupled with scotophases of specific duration.     

Seasonal modulation of diurnal food consumption in Indian songbirds

Seasonal changes in daily food consumption have a direct bearing with energy requirement of bird that is in turn associated with life history stage of birds. We compared seasonal changes in daily food intake in adult male migratory redheaded bunting (Emberiza bruniceps) that over winters in Indian subcontinent with those in non-migratory blackheaded munia to reiterate the same. We also compared daily food eating pattern (DFEP) in wintering blackheaded and redheaded buntings, closely related Emberizidae finches to establish circadian nature of feeding behavior and how it varied at species level. The birds were held under short days (8L:16D; 8 h of light and 16 h of darkness) and two hourly food consumption was measured to profile their DFEP. Further, we extended the study to establish how the circadian pattern of food consumption varied depending on birds’ physiological state and effect of photoperiod in adult male redheaded buntings. Redheaded buntings DFEP and locomotor activity were compared in pre-migratory months of February (spring) and September (autumn). The results suggest that September (photorefractory) birds exhibit clear bimodality in their feeding behavior as compared to (photosensitive) birds in February. Another experiment compared bird’s DFEP held under short (8L:16D) and long (16L:8D) days for 5 weeks and suggested that under long days, prolonged hours of photophase render adaptive advantage to birds for positive energy budgeting. The present study clearly establishes the circadian nature of feeding behavior and that it modulates over seasons. The bimodal i.e. morning and evening peaks of food consumption suggest morning–evening food entrainable oscillators, however this needs to be investigated with mechanistic approach in future studies.     

Geographic variation in basal thermogenesis in little buntings: Relationship to cellular thermogenesis and thyroid hormone concentrations

Acclimatization to different ambient conditions is an essential prerequisite for survival of small passerine birds. Long-distance migration and winter acclimatization induce similar physiological and biochemical adjustments in passerines. To understand metabolic adaptations, the resting metabolic rate (RMR), the thermogenic properties of mitochondria in liver and muscle, and the activity of thyroid hormones were examined in field-captured little buntings (Emberiza pusilla) between Southeastern (Wenzhou) and Northeastern (Qiqihar) China from March to May in 2008 during their migration. Twelve birds were trapped from March to April in Wenzhou region, Zhejiang Province (27°29′N, 120°51′E) and eleven birds originated from April to May in Qiqihar region, Heilongjiang Province (47°29′N, 124°02′E). We found that RMRs of little buntings were significantly higher in Qiqihar than in Wenzhou. Consistently, mitochondrial state-4 respiration capacities and cytochrome c oxidase activities (COX) in liver and muscle, and circulating levels of plasma triiodothyronine (T₃) of little buntings were also significantly higher in Qiqihar than in Wenzhou. Variation in metabolic biochemical markers of liver and muscle, such as state-4 respiration and COX, and variation in thyroid hormone levels were correlated with variation in RMR. There was also a positive relationship between T₃ and metabolic biochemical markers. Little buntings mainly coped with a cold environment by enhancing thermogenic capacities through enhanced respiratory enzyme activities and plasma T₃. These results support the view that the primary means by which small birds meet energetic challenges of cold conditions is through metabolic adjustments.