Elsevier

Environmental Pollution

Volume 249, June 2019, Pages 904-909
Environmental Pollution

Intensity dependent disruptive effects of light at night on activation of the HPG axis of tree sparrows (Passer montanus)

https://doi.org/10.1016/j.envpol.2019.03.008Get rights and content

Highlights

  • Artificial night light is a disruptor of the reproductive endocrine process of wild birds.

  • Low intensity night light accelerates the activation of HPG endocrine axis of tree sparrow.

  • High intensity night light retards the activation of HPG endocrine axis of tree sparrow.

Abstract

Artificial light at night (ALAN) has become increasingly recognized as a disruptor of the reproductive endocrine process and behavior of wild birds. However, there is no evidence that ALAN directly disrupt the hypothalamus-pituitary-gonadal (HPG) axis, and no information on the effects of different ALAN intensities on birds. We experimentally tested whether ALAN affects reproductive endocrine activation in the HPG axis of birds, and whether this effect is related to the intensity of ALAN, in wild tree sparrows (Passer montanus). Forty-eight adult female birds were randomly assigned to four groups. They were first exposed to a short light photoperiod (8 h light and 16 h dark per day) for 20 days, then exposed to a long light photoperiod (16 h light and 8 h dark per day) to initiate the reproductive endocrine process. During these two kinds of photoperiod treatments, the four groups of birds were exposed to 0, 85, 150, and 300 lux light in the dark phase (night) respectively. The expression of the reproductive endocrine activation related TSH-β, Dio2 and GnRH-I gene was significantly higher in birds exposed to 85 lux light at night, and significantly lower in birds exposed to 150 and 300 lux, relative to the 0 lux control. The birds exposed to 85 lux had higher peak values of plasma LH and estradiol concentration and reached the peak earlier than birds exposed to 0, 150, or 300 lux did. The lower gene expression of birds exposed to 150 and 300 lux reduced their peak LH and estradiol values, but did not delay the timing of these peaks compared to the control group. These results reveal that low intensity ALAN accelerates the activation of the reproductive endocrine process in the HPG axis, whereas high intensity ALAN retards it.

Introduction

While the natural photoperiod is an important cue for regulating physiological processes of birds (Gwinner, 2003, Wingfield, 1993), artificial light at night (ALAN) has been increasingly recognized as a type of pollution affecting the physiological processes of wild birds (Dominoni et al., 2013, Ouyang et al., 2017, Raap et al., 2016, Schoech et al., 2013, Zhang et al., 2014). The hypothalamic–pituitary–gonadal (HPG) axis regulating the seasonal reproductive behavior of vertebrate animals is particularly sensitive to disruption by ALAN (Dawson, 2015, Sower et al., 2009), because the activation of the HPG endocrine axis in temperate birds is stimulated by the day length increase in spring (Dawson et al., 2001, Wingfield, 1993).

The general physiological cascade of the HPG axis activation in birds is as follows: increasing day length in early spring is sensed by photoreceptors such as Opsin5 in the hypothalamus (Halford et al., 2009, Nakane et al., 2010), which promote the expression of the thyroid stimulating hormone β subunit gene (TSH-β) in the pars tuberalis of the pituitary, which in turn leads to synthesis of thyroid stimulating hormone (TSH). TSH then promotes the synthesis of deiodinase II (Dio2) in the medial basement of the hypothalamus to catalyze the transformation of tetraiodothyronine (T4) into triiodothyronine (T3) in the hypothalamus, where T3 promotes the secretion of GnRH-I (Yoshimura et al., 2003). GnRH-I stimulates the synthesis and release of luteinizing hormone (LH) and follicle stimulating hormone (FSH) in the pituitary (Pawson and McNeilly, 2005). These two hormones induce gonadal maturation, which initiates reproductive behavior by secreting testosterone (T) in male birds or estradiol (E2) in female birds (Lam and Farner, 1976, Palmer and Bahr, 1992).

A number of studies have found that the timing of seasonal reproductive processes differs between birds exposed to ALAN and those in areas with little or no ALAN (de Jong et al., 2015, de Molenaar et al., 2006, Dominoni et al., 2013, Kempenaers et al., 2010, Schoech et al., 2013). Given the central role of day length in regulating the HPG axis, one hypothesis to explain these findings is that ALAN disrupts HPG axis activation by altering day length, thereby modifying the timing of reproductive processes. LH, testosterone and estradiol secretion in wild bird species such as European blackbirds (Turdus merula), Florida scrub jay (Aphelocoma californica) and tree sparrow (Passer montanus) have been found to be affected by ALAN (Dominoni et al., 2013, Partecke et al., 2005, Schoech et al., 2013, Zhang et al., 2014). Dominoni et al. (2013) found that testis development was much earlier, and that the testosterone level was lower, in European blackbirds exposed to ALAN than in those that were not exposed to ALAN. Schoech et al. (2013) found that low intensity ALAN reduced the secretion of LH, T, and E2 in the Florida scrub jay. Zhang et al. (2014) found that the plasma LH levels of tree sparrows exposed to ALAN increased earlier, but had lower peak levels, compared to those that were not exposed to ALAN.

Although studies in controlled conditions generally find that ALAN affects the timing of seasonal reproductive endocrine processes, they have not demonstrated that it does this by directly stimulating the hypothalamus-pituitary-gonadal axis. Therefore, the possibility that ALAN affects seasonal reproduction by influencing other processes, such as foraging and social interactions (Davies and Deviche, 2014), cannot be excluded. There is a need to demonstrate that ALAN directly disrupts the physiological cascade of the HPG axis. The hypothalamus, the controlling organ of the HPG axis, is directly stimulated by light, therefore investigating the effect of ALAN on reproductive endocrine activation in the hypothalamus is necessary to demonstrate a direct effect of ALAN on the reproductive rhythm of wild birds. In addition, variation in ALAN intensity is a potentially important factor that has not been paid much attention. Most available studies have investigated the effect of a single light intensity on the reproductive endocrine axis (Dominoni et al., 2013, Schoech et al., 2013, Zhang et al., 2014). However, with ALAN intensity increasing (Falchi et al., 2016, Kyba et al., 2017) and ongoing advances in lighting technology, it is important to investigate if different levels of artificial light intensity have the same, or different, effects. If the latter, it may be possible to identify ALAN intensities that are least disruptive to birds.

We experimentally investigated whether ALAN, and its intensity, affect photoperiod induced reproductive endocrine activation of the HPG axis of wild tree sparrows (Passer montanus). The tree sparrow is a widespread passerine in urban and rural habitats that has a typical photoperiod stimulated HPG axis endocrine process (Zhang et al., 2014). Our previous field and laboratory studies have found that ALAN disrupts the pituitary hormone (LH) and gonadal hormone (testosterone and estradiol) rhythm of this species (Zhang et al., 2014), which implies that it could also disrupt the hypothalamic endocrine process. The synthesis of TSH-β, Dio2 and GnRH-I, key proteins or peptides regulating the activation of reproduction in hypothalamus, is stimulated by light. Therefore, we used TSH-β, Dio2 and GnRH as indicators of reproductive endocrine activation in the hypothalamus to compare the expression of these indicators in wild tree sparrows under different ALAN intensities. We also analyzed pituitary hormone LH and gonadal hormone estradiol secretion patterns in plasma under different night light intensities to evaluate whether the effects of ALAN on the hypothalamus affects pituitary and gonadal hormone secretion.

Section snippets

Experimental design

Tree sparrows were captured in a rural area of Beijing in December 2016 with mist-nets. We used climate chambers (Model RXZ-500C, Ninbo Jiangnan) for the experiment. Chambers were 73 cm wide, 77.5 cm deep, and 190 cm high, with a side-panel, adjustable, white, cold light source. To avoid the potential variation between the sexes we only used females in experiments. Forty-eight adult female tree sparrows were randomly assigned into four artificial climate chambers (12 birds per chamber). Birds

Differences in hypothalamic gene expression among treatment groups

The expression of TSH-β, Dio2 and GnRH-1 genes after the first day of the16L:8D photoperiod treatment differed significantly among treatment groups (TSH-β: one way ANOVA, F3, 20 = 130.86, P < 0.001; Dio2: one way ANOVA, F3, 20 = 352.25, P < 0.001; GnRH-I: one way ANOVA, F3, 20 = 213.57, P < 0.001) (Fig. 1). According to Turkey’s HSD post hoc test, the mean TSH-β gene expression level of the 85 lux group was significantly higher than that of the other treatment groups (P < 0.001), that of the

Discussion

After the first day of 16L:8D photoperiod treatment, the expression of TSH-β, Dio2 and GnRH-I genes in the hypothalamus of birds exposed to 85 lux in dark phase was significantly higher than that in birds exposed to 150 and 300 lux in dark phase. This indicates that the long light photoperiod induced HPG axis activation of the birds increased in the 85lux group, and decreased in the 150 and 300 lux groups, relative to the control group. These results reveal that ALAN influences the activation

Conclusions

ALAN directly affected the expression of genes responsible for the secretion of endocrine reproductive hormones in the hypothalamus of tree sparrows and the effects varied with the intensity of artificial light to which birds were exposed. Low light intensity both increased and advanced gene expression whereas exposure to higher light intensities suppressed gene expression. This suggests that exposure to low intensity ALAN may advance laying in wild birds but exposure to high intensity ALAN

Acknowledgement

This work was supported by the National Natural Science Foundation of China (Nos. 30900181), and the National Training Program of Innovation and Entrepreneurship for Undergraduates (GCCX2016110024).

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