Anthropogenic noise is associated with telomere length and carotenoid-based coloration in free-living nestling songbirds

Highlights

• Loud noise was related to short telomeres among small, but not large, brood members.

• Variance in noise levels was associated with carotenoid-based plumage traits.

• Carotenoid hue was positively related to telomere length.

• Noise levels were not correlated with body mass, hatching success or fledging success.

• Detecting deleterious effects of noise may depend on identifying sensitive groups.

Abstract

Growing evidence suggests that anthropogenic noise has deleterious effects on the behavior and physiology of free-living animals. These effects may be particularly pronounced early in life, when developmental trajectories are sensitive to stressors, yet studies investigating developmental effects of noise exposure in free-living populations remain scarce. To elucidate the effects of noise exposure during development, we examined whether noise exposure is associated with shorter telomeres, duller carotenoid-based coloration and reduced body mass in nestlings of a common urban bird, the great tit (Parus major). We also assessed how the noise environment is related to reproductive success. We obtained long-term measurements of the noise environment, over a ∼24-h period, and characterized both the amplitude (measured by LA_eq, LA_90, LA₁₀, LA_max) and variance in noise levels, since more stochastic, as well as louder, noise regimes might be more likely to induce stress. In our urban population, noise levels varied substantially, with louder, but less variable, noise characteristic of areas adjacent to a highway. Noise levels were also highly repeatable, suggesting that individuals experience consistent differences in noise exposure. The amplitude of noise near nest boxes was associated with shorter telomeres among smaller, but not larger, brood members. In addition, carotenoid chroma and hue were positively associated with variance in average and maximum noise levels, and average reflectance was negatively associated with variance in background noise. Independent of noise, hue was positively related to telomere length. Nestling mass and reproductive success were unaffected by noise exposure. Results indicate that multiple dimensions of the noise environment, or factors associated with the noise environment, could affect the phenotype of developing organisms, that noise exposure, or correlated variables, might have the strongest effects on sensitive groups of individuals, and that carotenoid hue could serve as a signal of early-life telomere length.

Introduction

Anthropogenic environments present organisms with complex mosaics of highly developed and less disturbed habitat, in which novel stressors are experienced (Gaston et al., 2013; Swaddle et al., 2015; Bauerová et al., 2017). Anthropogenic noise is one such stressor that may seriously interfere with animal behaviors, with cascading effects on health status and fitness (Barber et al., 2010; Kight and Swaddle, 2011; Swaddle et al., 2015; Shannon et al., 2016; Kleist et al., 2018). In habitats with high levels of anthropogenic noise, sounds and signals no longer propagate in the same way through the environment, with implications for foraging, vigilance, and communication (Leonard and Horn, 2005, 2008; Quinn et al., 2006; Kight and Swaddle, 2011; Narango and Rodewald, 2016). Moreover, innocuous anthropogenic noises may be perceived as stressors, and consistent activation of stress responses may result in chronic stress and pathology (Blickley et al., 2012; Tennessen et al., 2014; Kleist et al., 2018).

Exposure to loud noise may affect animals across life history stages (Francis and Barber, 2013), and may have particularly strong effects early in life, when the phenotype remains sensitive to organizational effects (Metcalfe and Monaghan, 2001; Monaghan, 2008). A growing number of studies on developing animals document effects of noise exposure on phenotypic traits, including body condition, oxidative status, glucocorticoid and haptoglobin levels, and growth and metabolic rates (Potvin and MacDougall-Shackleton, 2015; Brischoux et al., 2017; Davies et al., 2017; Raap et al., 2017; Injaian et al., 2018a, b). However, the mechanisms underlying phenotypic effects of early-life stress exposure in general, and anthropogenic noise exposure in particular, remain poorly understood.

One mechanism that may link later-life fitness effects to early-life stress exposure is telomere loss. Telomeres are conserved repeats of nucleotide sequences that cap chromosomes and protect coding DNA from damage and malfunction (Monaghan and Haussmann, 2006; Haussmann et al., 2012; Monaghan, 2014). Telomeres shorten upon cellular division, with rapid rates occurring during development in association with rapid growth (Heidinger et al., 2012). Once reduced beyond a threshold length, telomere shortening triggers cellular senescence. Shorter telomeres have been related to stress exposure, increased biomolecular aging rates, and pathology (Monaghan, 2014 for review). On a related vein, faster shortening of telomeres is correlated with disease and lower survival prospects (Haussmann et al., 2005; Heidinger et al., 2012; Boonekamp et al., 2014; Wilbourn et al., 2018).

Early-life noise exposure may also affect other condition-dependent traits, such as plumage pigmentation, with potential later-life effects on mating and reproductive success. Carotenoid-based pigmentation is a common sexually-selected trait in vertebrates, which is responsible for red, yellow and orange coloration in integumentary tissues (McGraw, 2006). Carotenoids must be obtained from the diet, since they cannot be synthesized de novo by animals (Isaksson, 2009), and may serve as antioxidants, meaning that depositing carotenoids in the skin or feathers may tradeoff against combating oxidative stress (Alonso-Alvarez et al., 2004, 2008; McGraw, 2006). Thus, increased stress levels associated with noise exposure may reduce the intensity of carotenoid-based coloration. Moreover, if carotenoid-based coloration is sensitive to stressors, such as loud noise, then coloration may serve as a visual signal of associated declines in physiological state, such as telomere loss and reduced body condition. Indeed, the role of carotenoids as antioxidants is debated, but their condition-dependence is well-established, and researchers have proposed that carotenoid-based pigmentation could serve as a bioindicator trait for environmental stress exposure (Hill, 1991, 1995; Eeva et al., 1998; McGraw, 2006).

Past studies demonstrate that early-life stress associated with factors such as sibling competition (Nettle et al., 2013, 2015; Stier et al., 2015), environmental conditions at high elevations (Stier et al., 2016), and nutritional stress (Nettle et al., 2017), can accelerate telomere shortening during development. In addition, great tit (Parus major) nestlings in urban areas were found to have shorter telomeres than those in rural areas (Salmón et al., 2016). Finally, three recent studies report negative effects of anthropogenic noise exposure on the telomere length of young birds (Meillère et al., 2015; Dorado-Correa et al., 2018; Injaian et al., 2019).

However, the association between early-life noise exposure and the expression of carotenoid-based pigmentation remains unexplored. Moreover, noise environments are multidimensional, and past studies have incompletely captured this complexity since they generally rely on single types of manipulations or short-term measurements of noise amplitude, thus ignoring patterns of temporal variance in noise (Gill et al., 2015). In addition to the amplitude of noise, variance in the noise environment may also significantly affect the phenotypic traits of animals, with ramifications for community dynamics and fitness. More variable noise regimes may be more likely to activate stress responses and result in phenotypic changes that have fitness consequences, whereas organisms might more readily habituate to consistent noise regimes (Blickley et al., 2012; Gill et al., 2015; Injaian et al., 2018b).

We explored the hypothesis that exposure to anthropogenic noise negatively affects telomere length, carotenoid-based pigmentation, and body mass in great tit (Parus major) nestlings, and also assessed the potential for duller carotenoid-based pigmentation to signal telomere shortening and reduced body mass. We obtained relatively long-term measurements of the noise environment (across an ∼24-h period), comprehensively quantified the noise environment during the nestling period, and assessed whether more variable, or well as louder noise environments, have deleterious effects on nestlings. In addition, we evaluated whether phenotypic associations with the noise environment are modified by a variable that may affect susceptibility to environmental stress, nestling size rank within a brood. Nestling size rank has been shown to affect competitive dynamics (Nettle et al., 2013), and we previously found that nestling size rank was associated with shorter telomere length in nestling great tits, whereas nestling sex and mass were not (Grunst et al., 2019a). Finally, we tested the hypothesis that reproductive success is reduced in loud, or variable, noise environments.