Dose‐response effects of light at night on the reproductive physiology of great tits (Parus major): Integrating morphological analyses with candidate gene expression

Abstract

Artificial light at night (ALAN) is increasingly recognized as a potential threat to wildlife and ecosystem health. Among the ecological effects of ALAN, changes in reproductive timing are frequently reported, but the mechanisms underlying this relationship are still poorly understood. Here, we experimentally investigated these mechanisms by assessing dose‐dependent photoperiodic responses to ALAN in the great tit (Parus major). We individually exposed photosensitive male birds to one of three nocturnal light levels (0.5, 1.5, and 5 lux), or to a dark control. Subsequent histological and molecular analyses on their testes indicated a dose‐dependent reproductive response to ALAN. Specifically, different stages of gonadal growth were activated after exposure to different levels of light at night. mRNA transcript levels of genes linked to the development of germ cells (stra8 and spo11) were increased under 0.5 lux compared to the dark control. The 0.5 and 1.5 lux groups showed slight increases in testis size and transcript levels associated with steroid synthesis (lhr and hsd3b1) and spermatogenesis (fshr, wt1, sox9, and cldn11), although spermatogenesis was not detected in histological analysis. In contrast, all birds under 5 lux had 10 to 30 times larger testes than birds in all other groups, with a parallel strong increase in mRNA transcript levels and clear signs of spermatogenesis. Across treatments, the volume of the testes was generally a good predictor of testicular transcript levels. Overall, our findings indicate that even small changes in nocturnal light intensity can increase, or decrease, effects on the reproductive physiology of wild organisms.

Artificial light at night as an environmental pollutant: An integrative approach across taxa, biological functions, and scientific disciplines

“…A major aim of our special issue was to reveal the multitude of molecular, physiological, and behavioral mechanisms that light pollution can affect. At the molecular and physiological level, these and previous papers have shown that ALAN can alter patterns of gene expression (Bedrosian, Galan, Vaughn, Weil, & Nelson, 2013;Dominoni et al, 2018;Fonken & Nelson, 2014;Shuboni & Yan, 2010), hormone secretion (Alaasam et al, 2018;de Jong et al, 2016;Dominoni, Goymann, Helm, & Partecke, 2013;Ouyang, Davies, & Dominoni, 2018), body temperature (Kumar et al, 2018), energy expenditure (Welbers et al, 2017), immune function (Bedrosian, Fonken, Walton, & Nelson, 2011;Cissé, Russart, & Nelson, 2017;Fonken, Lieberman, Weil, & Nelson, 2013), and oxidative stress (McLay et al, 2018;Navara & Nelson, 2007). Given, such extensive changes in the underlying physiology, it comes with no surprise that an impressive array of behavioral effects of ALAN have been shown.…”

“…When not possible, light emissions from streetlamps should be shielded so that light is only directed to the ground and not to the sky. Moreover, light has clear dose-dependent effects on many behavioral and physiological responses (see for instance Dominoni et al (2018) in the special issue as well as Brüning, Hölker, Franke, Preuer, and Kloas (2015) and de Jong et al (2016)). Thus, artificial light should be tuned to the intensity necessary to render an area visible to the human eye, while any excess lighting should be avoided.…”

Artificial light at night, in interaction with spring temperature, modulates timing of reproduction in a passerine bird

“…We have previously shown that in a passerine bird species, the Great Tit ( Parus major ), ALAN can affect both the timing of gonadal maturation (Dominoni et al. ) as well as that of the ultimate reproductive decision, egg laying (de Jong et al. ).…”

The preference and costs of sleeping under light at night in forest and urban great tits

“…Birds use light cues for synchronising their biological rhythms [5] and ALAN can alter their photoperiodic perception [6][7][8][9]. Consequently, ALAN can affect the timing of reproductive physiology and behaviour [8,10,11], timing of dawn singing [10,12,13] and sleep behaviour [14] of free-living passerine songbird species. Experimental studies on captive songbirds have confirmed work in the wild [7,15].…”