The rapid expansion of urbanization has led to widespread exposure of wild birds to intensive light at night (LAN). While previous studies have established LAN-induced cognitive impairment in birds, the underlying neurobiological mechanisms remain poorly understood. We hypothesized that LAN exposure impaired cognitive function of birds potentially through neurodegeneration, metabolic dysregulation and neuroinflammatory responses in the telencephalon. Using Zebra Finches (Taeniopygia guttata) as an avian model, under 16L:8D photoperiods, we compared associative learning and memory abilities and neurobiological parameters between experimental groups exposed to dim light at night (LAN) versus nocturnal darkness (CTR). Compared to the CTR birds, the LAN-exposed birds exhibited significantly lower learning and memory performances, reduced neuron density and simplified dendritic morphology in the telencephalons. The key energy metabolic substrates (cholic acid, CTP, D-mannose-6-phosphate) and neuroprotective agents (trehalose, menaquinone, L-gulono-1,4-lactone) in the telencephalons of LAN-exposed birds showed depletion, while oxidative stress markers (methionine sulfoxide) and inflammatory mediators (cis-gondoic acid) exhibited elevation. The neurotransmitter dopamine and histamine metabolic pathway were disrupted in the LAN-exposed birds. The microglias were activated with pro-inflammatory IL-1β and IL-6 levels increasing and anti-inflammatory IL-10 decreasing in the telencephalons of the LAN-exposed birds. These findings indicate a potential mechanistic pathway whereby dim light exposure at night can induce neuroinflammation through oxidative stress-mediated microglial activation, energy metabolism and neurotransmitter homeostasis disruption, ultimately leading to neurodegeneration in the telencephalons of birds.
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Open Access
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Embryonic development is a critical period for phenotype formation. Environmental variation during embryonic development can induce changes in postnatal phenotypes of animals. The thyroxine secretion and aerobic metabolic activity of small birds are important phenotypes closely related to their winter survival. In the context of climate change, it is necessary to determine whether temperature variation during incubation in birds leads to developmental plasticity of these cold responsive phenotypes. We incubated Japanese Quail (Coturnix japonica) eggs at 36.8 ℃, 37.8 ℃, and 38.8 ℃, and raised the chicks to 35-day old at 22 ℃ with same raising conditions, then all the quails were exposed to gradually temperature dropping environment (from 15 ℃ to 0 ℃). After cold treatment, serum T3 level, resting metabolic rate, skeletal muscle and liver metabolomes of the birds were measured. The serum T3 levels were significantly lower in the 38.8 ℃ group and significantly higher in the 36.8 ℃ group compared to the 37.8 ℃ group. The metabolic rate in the 38.8 ℃ group was significantly lower compared to the 37.8 ℃ group. Compared with the 37.8 ℃ group, metabolites involved in the tricarboxylic acid cycle in the liver were significantly lower in the 38.8 ℃ group, and metabolites related to lipid oxidation metabolism and fatty acid biosynthesis were significantly lower in the skeletal muscles in the 38.8 ℃ group but significantly higher in the 36.8 ℃ group. These results indicate that incubation temperature variation can lead to developmental plasticity in cold responsive physiological phenotypes. Higher incubation temperature may impair the capacity of birds coping with cold challenge.
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Night lighting has been shown to affect wild animals. To date, the effects of night lighting on the metabolic homeostasis of birds that spend short time in urban environments remain unclear. Using model bird species Zebra Finch (Taeniopygia guttata), we investigated the effects of short-term night lighting on liver transcriptome, blood glucose, triglyceride, and thyroxine (T4 and T3) levels in birds exposed to two different night lighting duration periods (three days and six days). After three days of night lighting exposure, the expression of genes involved in fat synthesis in the liver was upregulated while the expression of genes involved in fatty acid oxidation and triglyceride decomposition was downregulated. There was also a reduction in blood triglyceride, glucose, and T3 concentrations. However, after six days of night lighting, the expression of genes associated with fatty acid decomposition and hyperglycemia in the liver was upregulated, while the expression of genes involved in fat synthesis was downregulated. Simultaneously, blood glucose levels and T3 concentration increased. These findings indicate that short-term exposure to night lighting can disrupt the lipid and glucose metabolism of small passerine birds, and longer stopovers in urban area with intense night lighting may cause birds to consume more lipid energy.
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The egg yolks of birds contain most of the maternally derived materials required for embryo development and are an important factor influencing embryo development and offspring viability. Individual variation in egg-laying date frequently occurs in passerines inhabiting highly seasonal environments. Females laying in early and late stages of the breeding season encounter different environment temperatures and food conditions, which can affect the levels of metabolities in their bodies, thereby altering the transmission of these materials to the eggs. We test a hypothesis that yolk small molecule compounds of Asian Short-toed Lark (Alaudala cheleensis) could vary between early (mid-May) and late (mid-June) broods. Using the UHPLC-MS/MS method, 683 compounds belonging to 21 compound groups are detected in the yolks. The contents of 18 compounds are significantly different between early and late broods. Ten differential compounds are significantly higher in the early laid eggs, among which γ-aminobutyric acid, creatine, prostaglandins, palmitoleic acid, linoleic acid, and trans linoleic acid are related to low environment temperature response. The eggs laid in late stage exhibit significantly higher levels of 5-L-glutamyl-L-alanine and γ-glutamate-leucine, 1,3-dimethyluric acid and mannose, which may be attributed to females in the late group consuming more insects. We suggest conducting a comprehensive investigation to reveal the yolk small molecule compounds mediated maternal effects on offspring phenotypes under varying ecological conditions.
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In high latitude grassland habitats, altricial nestlings hatching in open-cup nests early in the breeding season must cope with cold temperature challenges. Thyroid hormones (triiodothyronine, T3 and thyroxine, T4) and corticosterone play a crucial role in avian thermoregulation response to cold. Investigating the endocrine response of altricial nestlings to temperature variation is important for understanding the adaptive mechanisms of individual variation in the timing of breeding in birds.
We compared nest temperature, ambient temperature, body temperature, plasma T3, T4 and corticosterone levels in Asian Short-toed Lark (Alaudala cheleensis) nestlings hatching in the early-, middle-, and late-stages of the breeding season in Hulunbuir grassland, northeast China.
Mean nest temperature in the early-, middle- and late-stage groups was−1.85, 3.81 and 10.23 ℃, respectively, for the 3-day-old nestlings, and 6.83, 10.41 and 11.81 ℃, respectively, for the 6-day-old nestlings. The nest temperature significantly correlated with body temperature, plasma T3, T4 and corticosterone concentrations of nestlings. Body temperature of 3-day-old nestlings in the early and middle groups was significantly lower than that of the late group, but there was no significant difference between the nestlings in the early and middle groups. The T4 and T3 concentrations and the ratio of T3/T4 of both 3- and 6-day-old nestlings in the early-stage group were significantly higher compared to the middle and late groups. The corticosterone levels of 3-day-old nestlings were significantly higher in the early-stage group compared to the middle- and late-stage groups.
Nestlings hatching early responded to cold temperature by increasing thyroid hormones and corticosterone levels even in the early days of post hatching development when the endothermy has not been established. These hormones may play a physiological role in neonatal nestlings coping with cold temperature challenges.
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Predicting the possibility of severe effects of global warming on animals is important for understanding the ecological consequences of climate change on ecosystem. Spring is the season during which birds have to physiologically prepare for the subsequent breeding period, and unusual spring temperature rising probably becomes a heat stress to the birds which have adapted to the low spring temperature. Therefore, it is necessary to understand the physiological effect of spring warming on the temperate birds.
Using the activities of blood anti-oxidative enzymes (SOD, CAT, GPx) and the concentrations of serum immunogloblins (IgA, IgY, IgM) as indicators, we compared the anti-oxidative and immune functions of Asian Short-toed Larks (Calandrella cheleensis) captured between 10 and 15 March, 2015 and housed under conditions of 21 ℃ and 16 ℃.
The SOD activities of birds in 21 ℃ group were significantly lower than those in 16 ℃ group on all the treatment days. The CAT activities of the birds in 21 ℃ group were significantly lower than those in 16 ℃ group on the 1st, 5th, 13th, 17 treatment days. The GPx activities of the birds in 21 ℃ group were signifthicantly lower than those in 16 ℃ group on the 1st, 13th and 17th, but significantly higher on the 21st treatment day. The IgA, IgY and IgM concentrations of birds in 21 ℃ group were significantly lower than those in 16 ℃ group on all the treatment days.
This study shows that spring temperature rising negatively influences antioxibative and humoral immune functions, which indicates that spring climate warming might reduce the fitness of the temperate passerine birds which have adapted to the low spring temperature.
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Timing of breeding season of temperate passerines has been considered to be adjusted to their food availability. There is little work to reveal the cell stress responses of the nestlings hatched asynchronized with the food abundance peak, which is important for understanding the physiological link between the timing of breeding and the fitness of offspring.
Using gene expression level of blood HSP70 and HSP90 as indicators, we compared the cell stress response of Asian Short-toed Lark (Calandrella cheleensis) nestlings hatched under conditions of low, mid or high food (grasshopper nymph) availability in 2017.
Nymph biomass, sample time and interaction of these two factors significantly influenced the blood gene expression level of HSP70 and HSP90 of Asian Short-toed Lark nestlings. HSP70 and HSP90 gene expression levels of the nestlings at 14:00 were significantly higher than those at 5:00. At either 5:00 or 14:00, the gene expression levels of HSP70 and HSP90 increase with the decrease of nymph biomass.
These results indicate that food availability is an important environment factor inducing cellular stress of Asian Short-toed Lark nestlings. The interactive effect of the nymph abundance and sample time on the HSPs response may be related with the daily temperature variation of the grassland. Over cell stress response may be one of physiological factor mediating the effect of food availability and the nestling's fitness.
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Global warming caused trophic mismatch has affected the breeding success, and even the survival, of some bird species. The ability of birds to accelerate their reproduction onset in the warmer spring could be critical to the survival of some species. The activation of the reproductive endocrine axis in birds is a key physiological process that determines the onset of reproduction. Could birds change the HPG axis endocrine rhythm under the temperature rising condition?
Using plasma LH level as an indicator of initiation of the reproductive endocrine and artificially controlling temperature, we compared variations in the timing of activation of the reproductive endocrine axis in response to temperature in two Chinese bird species, the Eurasian Skylark (Alauda arvensis) and the Great Tit (Parus major) at both the population and individual levels.
At the population level, temperature only significantly influenced LH level in the Eurasian Skylark, and had no significant effect on the LH levels in the Great Tit. Mean LH level of Eurasian Skylarks in the 20 ℃ group was higher than that of those in the 15 ℃ group throughout the experiment. Large individual variations in the timing of peak LH levels were observed in the high and the low temperature groups of both Eurasian Skylarks and Great Tits.
These results indicate that the effects of temperature differ among species. Meanwhile, there appears to be a degree of within population polymorphism in the timing of reproductive endocrine axis activation in some species. This polymorphism could provide the variation required for bird populations to cope with the possible change of their food peak under the climate warming condition.
Open Access
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Physiological preparation for reproduction in small passerines involves the increased secretion of reproductive hormones, elevation of the metabolic rate and energy storage, all of which are essential for reproduction. However, it is unclear whether the timing of the physiological processes involved is the same in resident and migrant species that breed in the same area. To answer this question, we compared temporal variation in the plasma concentration of luteinizing hormone (LH), testosterone (T), estradiol (E2), triiothyronine (T3) and body mass, between a migrant species, the Eurasian Skylark (Alauda arvensis) and a resident species, the Asian Short-toed Lark (Calandrella cheleensis), both of which breed in northeastern Inner Mongolia, China, during the 2014 and 2015 breeding seasons.
Twenty adult Eurasian Skylarks and twenty Asian Short-toed Larks were captured on March 15, 2014 and 2015 and housed in out-door aviaries. Plasma LH, T (males), E2 (females), T3 and the body mass of each bird were measured every six days from March 25 to May 6.
With the exception of T, which peaked earlier in the Asian Short-toed Lark in 2014, plasma concentrations of LH, T, E2 and T3 of both species peaked at almost the same time. However, Asian Short-toed Larks attained peak body mass earlier than Eurasian Skylarks. Plasma T3 concentrations peaked 12 days earlier than plasma LH in both species. Generally, plasma LH, T, E2, T3 and body mass, peaked earlier in both species in 2014 than 2015.
The timing of pre-reproductive changes in the endocrine system and energy metabolism can be the same in migrant and resident species; however, residents may accumulate energy reserves faster than migrants. Although migration does not affect the timing of pre-breeding reproductive and metabolic changes, migrant species may need more time to increase their body mass. T levels in resident species may be accelerated by higher spring temperatures that may also advance the pre-breeding preparation of both migrants and residents.
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