Artificial light at night (ALAN) affects the stress physiology but not the behavior or growth of Rana berlandieri and Bufo valliceps

https://doi.org/10.1016/j.envpol.2021.116775Get rights and content

Highlights

  • Artificial light at night (ALAN) alters tadpole physiology.

  • Anuran larvae up-regulate or down-regulate corticosterone release in response to ALAN.

  • Short term exposure to ALAN does not affect growth in tadpoles.

  • Short term exposure to ALAN does not affect tadpole behavior.

  • Ways to mitigate the effects of ALAN should be included in species management plans.

Abstract

Artificial light at night (ALAN) alters the natural light dark patterns in ecosystems. ALAN can have a suite of effects on community structure and is a driver of evolutionary processes that influences a range of behavioral and physiological traits. Our understanding of possible effects of ALAN across species amphibians is lacking and research is warranted as ALAN could contribute to stress and declines of amphibian populations, particularly in urban areas. We tested the hypothesis that exposure to constant light or pulsed ALAN would physiologically stress Rio Grande leopard frog (Rana berlandieri) and Gulf Coast toad (Bufo valliceps) tadpoles. We reared tadpoles under constant or pulsed (on and off again) ALAN for 14 days and measured corticosterone release rates over time using a non-invasive water-borne hormone protocol. ALAN treatments did not affect behavior or growth. Tadpoles of both species had higher corticosterone (cort) release rates after 14 days of constant light exposure. Leopard frog tadpoles had lower cort release rates after exposure to pulsed ALAN while toad tadpoles had higher cort release rates. These results suggest that short-term exposure to constant or pulsed light at night may contribute to stress in tadpoles but that each species differentially modulated their cort response to ALAN exposure and a subsequent stressor. This flexibility in the upregulation and downregulation of hypothalamic-pituitary-interrenal axis response may indicate an alternative mechanism for diminishing the deleterious effects of chronic stress. Nonetheless, ALAN should be considered in management and conservation plans for amphibians.

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).

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