Artificial light at night alters the sexual behaviour and fertilisation success of the common toad☆
Graphical abstract
Introduction
In recent decades, the rapid growth in the world’s population has led to a sharp increase in human activities necessary to support this growth. One consequence of the expansion of urban areas along with the development of transport infrastructures (Grimm et al., 2008; Gaston et al., 2013) is the major increase of light levels at night. In 2016, nearly 23% of the Earth’s surface, 88% of Europe and almost half of the United States experienced brightness levels higher than light levels at night in natural ecosystems (Falchi et al., 2016). Artificial Light At Night (ALAN) dramatically expanded. From 2012 to 2016, Earth’s artificially lit outdoor area grew by 2.2% per year, with a total radiance increase of 1.8% per year (Kyba et al., 2017). One of the major effects of ALAN is the disruption of the natural photoperiod, which is one of the most important cues for biological timing (Bradshaw & Holzapfel, 2010). Among all organisms, nocturnal species, which represent a large proportion of biodiversity, 28% of vertebrates and more than 60% of invertebrates (Hölker et al., 2010), are most likely to experience and to be affected by ALAN (Buchanan, 2006; Duffy et al., 2015; Desouhant et al., 2019). Nocturnal artificial light is known to affect a wide range of physiological and behavioural phenomena, such as migration (Van Doren et al., 2017), orientation (Tuxbury and Salmon, 2005), activity (e.g. Le Tallec et al., 2013; Pulgar et al., 2019; Touzot et al., 2019), foraging (Czarnecka et al., 2019), energy balance (e.g. Welbers et al., 2017; Touzot et al., 2019) and hormonal synthesis (e.g. Brüning et al., 2015; Newman et al., 2015). These effects on individuals have the potential to alter population dynamics (e.g. Gaston et al., 2014; Grubisic et al., 2017; Sanders et al., 2018).
Despite the evidence of profound effects of ALAN on life history traits across different taxonomic groups with important ecological consequences (e.g. Gaston and Bennie, 2014; Knop et al., 2017; Bennie et al., 2018), we still have little information on the direct effects of ALAN on the fitness of individuals although its assessments are key elements in conservation. Fitness, i.e. the average contribution to the gene pool of the next generation that is made by individuals of a specified genotype or phenotype in a given environment, is often estimated through measurements of mortality and breeding success. Most of the studies conducted to date focused on the effects of ALAN on the mortality component of fitness (e.g. Rodríguez et al., 2014; Willmott et al., 2018). The breeding component of fitness has been less examined, even if a growing number of studies (reviewed in Ouyang et al., 2018) reported that the timing and the physiology of seasonal reproductive processes differ between individuals living in lit areas and their conspecifics living in darker areas. Alterations of the period of functional development of reproductive organs, reproductive hormonal synthesis (estradiol, ketotestosterone), number of eggs produced by females, egg hatchling success, number of offspring and birth schedule in response to ALAN exposure were found in various taxa (mammals: Le Tallec et al., 2015; Robert et al., 2015, birds: Dominoni et al., 2013; de Jong et al., 2015, fishes: Brüning et al., 2018, Fobert et al., 2019 and insects: McLay et al., 2018; Willmott et al., 2018). On contrary, other studies have found no effect of ALAN on the time for copulation or between mating and laying egg, on the number of eggs or egg sacs laid and on sperm viability (e.g. Durrant et al., 2018; McLay et al., 2018; Willmott et al., 2018). A recent study investigating the influence of ALAN on the fertilisation success of fish, ultimately showed no effect (Fobert et al., 2019). The influence of ALAN on amphibian reproduction is still scarce, however effects of photoperiod modifications have been highlighted. The suppression of the dark period triggered a decrease of spermatocytes in male Asian toads, Bufo melanostictus (Biswas et al., 1978), and a severe reduction of sexual calls in male green frogs, Rana clamitans melanota, (Baker & Richardson, 2006).
In this context, we experimentally studied the effect of three ecologically relevant light intensities at night (0.01, 0.1 or 5 lux), which correspond to light levels measured in areas hosting amphibians (Secondi et al., 2017), on both the reproductive behaviour and the fertilisation success of male common toads, Bufo bufo. This nocturnal amphibian is one of the most common and ubiquitous amphibians in Europe, and can be a useful indicator of ecosystem health and function (Hilty and Merenlender, 2000). Moreover, the common toad is an explosive breeding species with a breeding period lasting only a few days, thus limiting the number of pairing opportunities (Wells, 1977). The operational sex ratio of this species is biased towards males, leading to scrambling competition among males to mate with a female. During the breeding season, common toads are frequently found in urban and peri-urban areas with wetlands (Beebee, 1979), especially small ones (ponds for instances) which are subjected to ALAN (Secondi et al., 2017). In addition, due to their high nocturnal visual sensitivity, amphibian activities, such as foraging and breeding, are expected to be affected by changes in night brightness (Buchanan, 2006; Grant et al., 2009; Yovanovich et al., 2017). We have previously shown that ALAN exposure decreased common toad activity during the night and increased allocation of energy to maintenance (Touzot et al., 2019). This suggested that breeding activities occurring at dusk or at night may be influenced by ALAN. Considering this, we predicted that (i) ALAN exposure would alter male breeding behaviour, particularly their ability to maintain pairing with a female, which is a costly activity for this species (Lengagne et al., 2007), (ii) these behavioural alterations could be due to changes in male testosterone concentrations, and (iii) ALAN exposure would reduce male fertilisation success.
Section snippets
Animal collection and housing conditions
A total of 60 male common toads were collected during the breeding season (8–9 March 2018) in La Burbanche, France (45°N, 5°E). This site was chosen for its low levels of ALAN regardless of weather conditions and the lunar phase (≤0.01 lux). Upon arrival at the animal care facility (EcoAquatron, University of Lyon), males were weighed (LAB 800-3000, precision: 0.1 g, B3C pesage, Sérénité) and housed individually in boxes (47 × 36 × 25 cm) containing a 15 cm section of PVC tubing (diameter
ALAN affected reproductive behaviours of males
Male body mass gain during ALAN exposure was on average of 10.66 ± 1.27 g in the control group (mean ± SEM) and did not significantly differ between the light treatments (see Appendix Supplementary Material S4 for details). At mating, on D13, male body mass, male SVL measurement and the ratio between male and female size did not significantly differed between the light treatments (see Appendix Supplementary Material S4 for details). For all light treatments, each male performed an amplexus with
Discussion
Here, we demonstrated that exposure to low but realistic light intensities at night during the breeding period alters both the mating behaviours and the fertilisation success of common toad males. Indeed, ALAN affected mating behaviour as male common toads previously exposed to ALAN needed several attempts to maintain a female in amplexus until clutch laying, although all males finally paired in our experimental setup. In line with this first result, the latency to pair successfully with a
Conclusion
Although some studies have investigated the effects of ALAN on the mortality component of fitness (Rodríguez et al., 2014; Van Doren et al., 2017; Willmott et al., 2018), reports of effects on the breeding component are still scarce, especially in amphibian species. This study showed that relevant nocturnal artificial light intensities can have a major effect on the breeding component of fitness of animals in the wild. Even if a reduction in fertilisation rate was observed at the rather high
CRediT authorship contribution statement
Morgane Touzot: Conceptualization, Investigation, Data curation, Formal analysis, Writing - original draft. Thierry Lengagne: Data curation, Writing - review & editing. Jean Secondi: Writing - review & editing. Emmanuel Desouhant: Formal analysis, Writing - review & editing. Marc Théry: Writing - review & editing. Adeline Dumet: Data curation. Claude Duchamp: Writing - review & editing. Nathalie Mondy: Conceptualization, Investigation, Data curation, Writing - review & editing.
Acknowledgements
We thank A. Clair, J. Ulmann and L. Averty for their technical assistance in the EcoAquatron; L. Guillard for his help with the setting up of LED ribbons; and Elsevier for English corrections.
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2022, Environmental PollutionCitation Excerpt :Specifically, disruptions to photoperiod can lead to a misalignment in circadian rhythms which cause mass gain and metabolic abnormalities (Fonken et al., 2010; Fonken and Nelson, 2014). Despite this, others have observed decreases in mass following ALAN exposure (Dananay and Benard, 2018), while others have found that ALAN has no impact on mass (Touzot et al., 2019, 2020). Understanding the impact of pollutants on size is important because size is often a proxy for fitness and can have significant effects on ecological interactions (Berven, 1990; Cabrera-Guzmán et al., 2013; Semlitsch et al., 1988).
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This paper has been recommended for acceptance by Wen Chen.