Artificial light at night (ALAN) affects the stress physiology but not the behavior or growth of Rana berlandieri and Bufo valliceps☆
Graphical abstract
Introduction
Artificial light at night (ALAN, Haim and Zubidat, 2015) is a significant threat to biodiversity (Gaston et al., 2019; Secondi et al., 2020; Seymoure et al., 2019) particularly in urban areas. Sources of ALAN include light trespass from streetlamps, lights on buildings, vehicles, and sky glow from cities (Aubé et al. (2016); Longcore and Rich, 2004; Navara and Nelson, 2007). Natural environmental daytime light levels range from 800 lx at sunset up to 100,000 lx on a clear day, while nighttime light levels range from 0.3 lx on a full moon night down to 0.001 lx on a clear, moonless, night (Hänel et al., 2018). Sources of ALAN can increase light levels many kilometers from urban centers (Kyba et al. (2017); Secondi et al., 2020) so ALAN also impacts rural areas adjacent to urban centers. Over 80% of the world population live in areas polluted by ALAN (Falchi et al., 2016), 40% of which experience constant ALAN (Swaddle et al., 2015), and Seymoure et al. (2019) estimate that over 50% and 75% of key biodiversity areas and Global protected rea units, respectfully, are affected by ALAN. With continued human population growth and urbanization, ALAN is estimated to be increasing at a rate of 6% yearly (Hoelker et al., 2010), and thus the impact of ALAN on organisms may be of great importance and potential negative effects may have significant ecological consequences and conservation implications (Gaston et al., 2019; Secondi et al., 2020; Seymoure et al., 2019).
Amphibian populations are experiencing global population declines (Clulow et al., 2014; Collins and Halliday, 2005; Grant et al., 2016) and ALAN may be contributing to their population declines, as ALAN affects the behavior, physiology, and development of many taxa (see reviews: Gaston et al., 2014; Longcore and Rich, 2004; Navara and Nelson, 2007; Secondi et al., 2020; Swaddle et al., 2015), but our understanding of the ecological impacts of ALAN is limited relative to that of other anthropogenic perturbations (Desouhant et al., 2019). ALAN affects amphibian behavior, physiology, and growth (Dananay and Benard, 2018; Gern et al., 1983; May et al., 2019; Wise and Buchanan, 2006). When exposed to 3.8–12.0 lx ALAN, adult grey treefrogs, Hyla chrysoscelis, reduce foraging (Buchanan, 1993) and adult red-back salamanders, Plethodon cinereus, exposed to ALAN from string lights (lux not reported but likely low light) reduce activity and foraging (Wise and Buchanan, 2006). Similarly, adult common green frogs, Rana clamitans, reduce advertisement calling when exposed to 52 lx–120 lx ALAN (Baker and Richardson, 2006). Constant light (lux not reported) affects the physiology of tiger salamanders, Ambystoma tigrinum, by disrupting normal oscillating melatonin rhythms associated with normal light/dark cycles (Gern et al., 1983). Larval leopard frogs, Rana pipiens (lux not reported; Eichler and Gray, 1976), and larval American toads, Bufo americanus (22 lx–1.3 lx; Dananay and Benard, 2018), metamorphosed faster and weighed less at metamorphosis when reared under constant light. Contrastingly, May et al. (2019) found larval wood frogs, Rana sylvatica, metamorphosed faster but weighed more at metamorphosis when exposed to 300 lx ALAN. Additionally, May et al. (2019) did not see an effect of ALAN on corticosterone release rates in R. sylvatica larvae, however ALAN affects glucocorticoid concentrations in other taxa (Ouyang et al., 2015). Understanding how ALAN affects amphibians is important, as ALAN may be potentially contributing to stress and declines of amphibian populations, particularly in urban areas.
Anuran larvae are likely stressed by ALAN as many species are nocturnal and have dark adapted eyes (Baker and Richardson, 2006), circadian rhythms are tied to natural light/dark cycles (Azzi et al., 2014; Botha et al., 2017; Ciarleglio et al., 2011) and changes to circadian rhythms can affect physiological processes (Fonken and Nelson, 2014). ALAN disrupts natural light/dark cycles (Falchi et al., 2016), and disrupts circadian rhythms (Bedrosian et al., 2013; Botha et al., 2017; Dominoni et al., 2013), which can alter glucocorticoid (GC) levels (Ouyang et al., 2015). The amphibian neuroendocrine response to a stressor involves the hypothalamic-pituitary-interrenal, HPI, axis (Cyr and Romero, 2009) and often results in increased circulating levels of corticosterone (cort), the main GC in amphibians (Forsburg et al., 2019; Idler, 1972), above normal “baseline” levels (Romero et al., 2009). A short-term elevation of circulating GCs can be advantageous as it mediates gluconeogenesis and mobilizes energy (Hau et al., 2016; Romero et al., 2009; Sapolsky et al., 2000), however unpredictable and long-term perturbations can lead to persistently elevated or down regulated (suppressed) GC levels which can be deleterious (Romero et al., 2009). Elevated levels of cort can reduce growth in amphibian larvae, alter tadpole morphology, and hasten metamorphosis (Crespi and Warne, 2013; Denver et al., 1998; Glennemeier and Denver, 2002a; Hu et al., 2008), and reduced mass at metamorphosis can affect growth and survivorship later in life (Cabrera-Guzman et al., 2013; Chelgren et al., 2006; Crespi and Warne, 2013; Earl and Whiteman, 2015; Rohr et al., 2013).
We can gain a better understanding of how individuals physiologically cope with changing environments by measuring cort release rates over time and by measuring how individuals respond to an acute stressor, such as agitation (Wikelski and Cooke, 2006). The physiological responses of individuals can give us insight into individual and population health (Dantzer et al., 2014; Gabor et al., 2018; Sheriff et al., 2011; Wikelski and Cooke, 2006) and may change over time or show flexibility as the environment changes. Hormone responses may be repeatable and or flexible. Hormone levels fluctuate from day to night and may change in response to variation in abiotic and biotic factors in a changing environment (Hau et al., 2016). Modulating hormonal responses help mediate behavior, physiology, and morphology in changing environments (Nelson, 2011), particularly glucocorticoid (GCs) responses, as they help to maintain energy needs in both predictable and unpredictable events (Sapolsky et al., 2000). Variation in circulating levels of GCs and hormonal and behavioral responses to changing environments have been observed both within and among individuals (reviewed in Hau et al., 2016) and this variation is mediated by phenotypic flexibility (Piersma and Drent, 2003). By repeatedly measuring hormones from the same individual over time using a non-invasive, water-borne, hormone collection protocol (Gabor et al., 2016), one can measure within and among individual variation of hormone levels and calculate the repeatability of hormone levels.
We explored the consequences of exposure to 190 lx–250 lx ALAN on the physiology and growth of two common anurans, the Gulf Coast toad (Bufo valliceps) and the Rio Grande leopard frog (Rana berlandieri), using laboratory experiments across three years. We also examined how ALAN affects the behavior of R. berlandieri. First, in 2017, we exposed pre-metamorphic Rana berlandieri tadpoles to different light conditions for 14 days to explore how ALAN affects corticosterone release rates, tadpole behavior, and growth. We then reared the tadpoles on a natural light cycle for an additional 7 days, post treatments, to explore if tadpoles recover from any effects of ALAN treatments. We then reared pre-metamorphic larval R. berlandieri and Bufo valliceps, in 2018 and 2019 respectfully, under a control light cycle for 7 days and then exposed them to an either pulsed ALAN or constant ALAN for 14 days to explore if tadpoles respond to a changing environment by altering cort release rates and to test if ALAN exposure affects growth. We hypothesized that both constant and pulsed ALAN would be a stressor for tadpoles and tadpoles cort release rates be affected by the light treatments.
Section snippets
Animal collection and husbandry
We collected portions of three Rio Grande leopard frog, Rana berlandieri, egg masses from a local pond in San Marcos, Hays Co., Texas (29.874695, −97.962733) on February 23, 2017, four R. berlandieri egg masses from the same pond on March 5, 2018, and collected several strands of eggs from four different groupings of Gulf Coast toad, Bufo valliceps, eggs from two different local ponds in San Marcos, Hays Co., Texas (29.874695, −97.962733 and 29.903373, −97.966839) on April 10, 2019. In each
2017 Rana berlandieri: reared under ALAN treatments then moved to control
All tadpoles survived to the end of the experiment and there was no significant treatment effect on mass (F2,42 = 0.566, p = 0.572), snout-vent-length (SVL) (F2,42 = 0.521, p = 0.811), tail height (TH) (F2,42 = 0.161, p = 0.852), or body condition (F2,42 = 2.563, p = 0.089). Tadpole activity did not differ across treatments (F2,42 = 01.459, p = 0.244). There was no significant interaction of treatment and time on cort release rates (F4,84 = 1.507, p = 0.208), though there were significant
Discussion
We explored how ALAN affects the physiology, growth, and behavior of Rio Grande leopard frog and Gulf Coast toad tadpoles. We found that exposure to environmentally relevant levels of constant or pulsed ALAN (190 lx–250 lx) did not affect growth of two species of tadpoles, nor the behavior of Rana berlandieri tadpoles, however, we did see elevated and suppressed baseline cort release rates. This indicates that tadpoles are affected by ALAN but their physiological response varies by species and
Conclusions
The results of this experiment support the hypothesis that both pulsed and constant ALAN act as a stressor for both R. berlandieri and B. valliceps tadpoles and contribute to our understanding of how ALAN affects amphibians. Interestingly, both species differentially modulated their cort response to ALAN exposure and a subsequent stressor. Such flexibility in the HPI axis response has not been found in other non-amphibian species and may indicate an alternative mechanism for diminishing the
Author contribution
Forsburg: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Resources, Writing – original draft, Writing – review & editing, Visualization, Supervision, Project administration, Funding acquisition, Guzman: Formal analysis, Investigation, Writing – review & editing, Gabor: Conceptualization, Methodology, Writing – review & editing, Supervision, Funding acquisition
Funding
This research was funded through Texas Ecolab grants to Z.R.F & C.R.G, a Texas Herpetological Society Grant in Research to Z.R.F., and a Texas State University Doctoral Research Support Fellowship to Z.R.F.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Thank you to members of the GASP lab for helpful comments and discussion. All protocols and housing were approved by the Institutional Animal Care and Use Committee of Texas State University (IACUC #201563714).
References (65)
- et al.
The spectral amplification effect of clouds to the night sky radiance in Madrid
J. Quant. Spectrosc. Radiat. Transf.
(2016) - et al.
Artificial light at night alters delayed-type hypersensitivity reaction in response to acute stress in Siberian hamsters
Brain Behav. Immun.
(2013) - et al.
Effects of lifetime exposure to artificial light at night on cricket (Teleogryllus commodus) courtship and mating behaviour
Anim. Behav.
(2017) Effects of enhanced lighting on the behaviour of nocturnal frogs
Anim. Behav.
(1993)- et al.
Validation of water-borne cortisol and corticosterone in tadpoles: recovery rate from an acute stressor, repeatability, and evaluating rearing methods
Gen. Comp. Endocrinol.
(2019) - et al.
Measuring night sky brightness: methods and challenges
J. Quant. Spectrosc. Radiat. Transf.
(2018) - et al.
Chapter two-glucocorticoid-mediated phenotypes in vertebrates: multilevel variation and evolution
Adv. Stud. Behav.
(2016) Effects of uneven-aged timber harvest on forest floor vertebrates in the Cascade Mountains of southern Washington. For
Ecol. Manag.
(2005)- et al.
The effect of intensified illuminance and artificial light at night on fitness and susceptibility to abiotic and biotic stressors
Environ. Pollut.
(2019) - et al.
Repeated thermal stressor causes chronic elevation of baseline corticosterone and suppresses the physiological endocrine sensitivity to acute stressor in the cane toad (Rhinella marina)
J. Therm. Biol.
(2014)
The reactive scope model—a new model integrating homeostasis, allostasis, and stress
Horm. Behav.
A framework to assess evolutionary responses to anthropogenic light and sound
Trends Ecol. Evol.
Conservation physiology
Trends Ecol. Evol.
The comparative biology of environmental stress: behavioural endocrinology and variation in ability to cope with novel, changing environments
Anim. Behav.
Circadian behavior is light-reprogrammed by plastic DNA methylation
Nat. Neurosci.
The effect of artificial light on male breeding season behaviour in green frogs, Rana clamitans melanota
Can. J. Zool.
Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina)
PloS One
Carryover aquatic effects on survival of metamorphic frogs during pond emigration
Ecol. Appl.
Perinatal photoperiod imprints the circadian clock
Nat. Neurosci.
Amphibian declines in the twenty-first century: why we need assisted reproductive technologies
Reproductive Sciences in Animal Conservation
Forecasting changes in amphibian biodiversity: aiming at a moving target
Philos. Trans. R. Soc. B
Environmental conditions experienced during the tadpole stage alter post-metamorphic glucocorticoid response to stress in an amphibian
Integr. Comp. Biol.
Identifying hormonal habituation in field studies of stress
Gen. Comp. Endocrinol.
Artificial light at night decreases metamorphic duration and juvenile growth in a widespread amphibian
Phil. Trans. Roy. Soc. Lond. B
Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation
Ecology
Mechanistic, ecological, and evolutionary consequences of artificial light at night for insects: review and prospective
Entomol. Exp. Appl.
Quantifying individual variation in behaviour: mixed-effect modelling approaches
J. Anim. Ecol.
Repeatability estimates do not always set an upper limit to heritability
Funct. Ecol.
Artificial light at night advances avian reproductive physiology
Phil. Trans. Roy. Soc. Lond.
Are commonly used fitness predictors accurate? A meta-analysis of amphibian size and age at metamorphosis
Copeia
The influence of environmental lighting on the growth and pro-metamorphic development of larval Rana pipiens
Dev. Growth Differ.
The new world atlas of artificial night sky brightness
Sci. Adv.
Cited by (17)
The hidden impact of an invasive predator: Chronic stress in common frog tadpoles
2024, Global Ecology and ConservationNoise and light pollution elicit endocrine responses in urban but not forest frogs
2024, Hormones and BehaviorEffects of anthropogenic light on anuran calling site
2023, Environmental PollutionArtifical light at night triggers slight transcriptomic effects on melatonin signaling but not synthesis in tadpoles of two anuran species
2023, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyUnder the influence of light: How light pollution disrupts personality and metabolism in hermit crabs
2023, Environmental PollutionCitation Excerpt :However, artificial light at night (ALAN) can mask seasonal and monthly fluctuations in sky brightness regimes and thus interfere with these cues. There is increasing evidence that ALAN can alter physiology (Forsburg et al., 2021; Luarte et al., 2016; Raap et al., 2016a; Zubidat et al., 2018), metabolism (Finch et al., 2020; Nelson, 2019; Raap et al., 2018a; Welbers et al., 2017), foraging (Davies et al., 2013; Farnworth et al., 2018) reproduction and mating behaviour (Ayalon et al., 2021; Botha et al., 2017; Touzot et al., 2019), often in a species specific manner (Amadi et al., 2021; Baskir et al., 2021; Brisbane and van den Burg, 2020; Polak et al., 2011), making understanding ALAN's impacts challenging. However, changes in physiology and behaviour could alter interspecific dynamics, having significant ecological consequences disrupting entire ecological communities (Bennie et al., 2018; Sanders et al., 2018, 2015).
Transcriptome-wide deregulation of gene expression by artificial light at night in tadpoles of common toads
2022, Science of the Total EnvironmentCitation Excerpt :Moreover, in the case of ALAN that disturbs the normal photoperiod, early stages, which have a relatively immature circadian system and incomplete differentiation of organs and tissues, may be particularly sensitive to rhythm disruptions through ALAN (Fonken and Nelson, 2016), making their study relevant. Finally, several studies have shown that the presence of ALAN induced numerous effects in tadpoles, especially bufonidae (Dananay and Benard, 2018; Forsburg et al., 2021), effects that can persist throughout life, and affect individual fitness at the adult stage (Metcalfe and Monaghan, 2001; Fonken and Nelson, 2016). Therefore, in the present study, we combined de novo transcriptome sequencing and assembly, and a controlled laboratory experiment to investigate the transcriptome-wide gene expression response using Illumina RNA-seq in common toad tadpoles following prolonged exposure to ALAN.
- ☆
This paper has been recommended for acceptance by Christian Sonne.