Exposure to artificial light at night increases innate immune activity during development in a precocial bird

https://doi.org/10.1016/j.cbpa.2019.04.002Get rights and content

Highlights

  • We exposed developing king quail (Excalfactoria chinensis) to weak artificial light at night (ALAN).

  • ALAN briefly increased the immune activity of king quail.

  • ALAN increased immune activity at different developmental timepoints for males and females.

Abstract

Humans have greatly altered Earth's night-time photic environment via the production of artificial light at night (ALAN; e.g. street lights, car traffic, billboards, lit buildings). ALAN is a problem of growing importance because it may significantly disrupt the seasonal and daily physiological rhythms and behaviors of animals. There has been considerable interest in the impacts of ALAN on health of humans and other animals, but most of this work has centered on adults and we know comparatively little about effects on young animals. We exposed 3-week-old king quail (Excalfactoria chinensis) to a constant overnight blue-light regime for 6 weeks and assessed weekly bactericidal activity of plasma against Escherichia coli – a commonly employed metric of innate immunity in animals. We found that chronic ALAN exposure significantly increased bactericidal activity and that this elevation in immune performance manifested at different developmental time points in males and females. Whether this short-term increase in immune activity can be extended to wild animals, and whether ALAN-mediated increases in immune activity have positive or negative fitness effects, are unknown and will provide interesting avenues for future studies.

Introduction

Humans have greatly altered the night-time photic environment from local to global scales via the production of artificial light at night (ALAN; e.g. street lights, lit buildings) (Falchi et al., 2016). ALAN is problematic because it can significantly disrupt the seasonal/daily physiological rhythms (e.g. immune and reproductive physiology; Swaddle et al., 2015) and behaviors (e.g. predator avoidance, foraging, mating; Kempenaers et al., 2010; Swaddle et al., 2015) of animals, including humans (Cho et al., 2015). Some animals avoid ALAN-rich areas or suffer significant fitness consequences from ALAN exposure, thereby rapidly selecting against some species and ultimately depleting biodiversity (Swaddle et al., 2015).

Among the diverse potential effects of ALAN on organisms, much attention has been paid to its health consequences (Navara and Nelson, 2007). Alterations to light-entrained biorhythms can impact disease exposure and susceptibility, as well as the activity of the immune system (Navara and Nelson, 2007) in a range of taxa (Bedrosian et al., 2011). In 2012, the American Medical Association House of Delegates went as far as adopting a policy statement on nighttime lighting, summarizing the deleterious effects of ALAN on a host of circadian-disruption- and melatonin-suppression-related health outcomes in humans (e.g. cancer, obesity, diabetes, depression; Blask et al., 2012).

Surprisingly, despite the wealth of work in and attention to this area, the majority of studies on ALAN and health have centered on adult animals (Moore and Siopes, 2000; Phillips et al., 2015). Growing young animals might be especially susceptible to ALAN-driven perturbations to metabolic, immunological, or tissue growth/repair systems (Fonken and Nelson, 2016). In human children, ALAN increases body mass (Pattinson et al., 2016) and suppresses melatonin secretion (Higuchi et al., 2014), which regulates both sleeping behavior and immunity. Similarly, ALAN was found to suppress immune activity in young Japanese quail (Coturnix japonica) (Moore and Siopes, 2000) and chickens (Gallus domesticus) (Kirby and Froman, 1991). However, a recent study found that ALAN significantly elevated levels of haptoglobin (an acute phase protein) in wild great tit (Parus major) nestlings, suggesting that further work is needed to refine our understanding of how ALAN affects immunological state in developing animals (Raap et al., 2016).

Here we experimentally tested the effect of ALAN exposure on the bacterial-killing response of developing king quail (Excalfactoria chinesis). We exposed 3-week-old quail to a constant overnight blue-light regime for 6 weeks and drew blood weekly to assess the ability of the plasma to kill microbes (e.g. Escherichia coli) ex vivo (i.e. bacterial-killing assay, which assesses basal innate immunocompetency; French and Neuman-Lee, 2012). Note that, while bactericidal activity is an integrated measure of basal innate immunity, other components not measured in this study may differ in their response to ALAN. We hypothesized that chronic ALAN exposure during development would weaken innate immunity compared to animals exposed to a regular daily light/dark cycle. Also, although prior work in very young nestling great tits found no sex differences in the immune effects of ALAN (Raap et al., 2016), we tested effects over a longer range of development (including sexual maturation) and thus hypothesized that males may be more immunocompromised by ALAN exposure than females due to photostimulation of immunosuppressive testosterone secretion (Koutsos and Klasing, 2014).

Section snippets

Study species

King quail are an ideal study species because they develop to adulthood quickly (in about 50–60 days; Pis and Luśnia, 2005), are amenable to captivity (Adkins-Regan, 2016), and are precocial (i.e., removing complex indirect, parental effects on chicks). This non-migratory species inhabits Old World (e.g. southeast Asia, Australia) coastal tropical and temperate grasslands that are dense with ground vegetation.

Pre-experiment

We artificially-incubated and hatched 41 king quail eggs. During egg incubation,

Results

Prior to the night-light manipulation, there were no differences in plasma bactericidal activity among any of the groups (Fig. 1, Table S1). We found that experimental ALAN exposure significantly increased the bactericidal capacity of plasma for both males and females compared to controls, but at different time points for each sex (Table 1). After 4 or 6 weeks of treatment, for females and males respectively, the plasma of ALAN-exposed birds had greater bactericidal activity than that of

Discussion

Counter to our predictions, we found no evidence that ALAN decreased immune activity during development in king quail. Instead, our findings likely indicate an ephemeral increase in immunocompetence during chronic experimental exposure to ALAN over development. Prior research suggests that extended photoperiod can compromise immune performance in both adult (Moore and Siopes, 2000) and juvenile birds (Kirby and Froman, 1991), but we found that the plasma of ALAN-exposed quail showed a superior

Ethics

This study was carried out with the approval of Arizona State University's IACUC, and complies with the National Institutes of Health guidelines for the care and use of laboratory animals.

Data accessibility

Data from this study are available in Dryad.

Competing interests

The authors declare no competing interests.

Funding

Financial support was provided by Barrett, the Honors College, at Arizona State University to CS and KJM.

Acknowledgements

We thank Karen Sweazea for helpful comments on prior manuscript drafts, and Devon Allred, Chris Carpenter, Melinda Weaver, Joey Barbera, Missy Tran, and Hannah MacKellar for assistance with the experiment. We appreciate the thoughtful feedback on an earlier draft of this paper by two anonymous reviewers.

Declaration of interest

The authors declare no conflict of interest.

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