With this chapter, I do not intend to cover all kinds of phenotypic changes or drivers. In fact, in many cases the causal relationship between a driver and a phenotypic change is not known or difficult to single out from the ocean of possible urban drivers. Thus, many studies of phenotypic changes are linked to urbanization per se rather than to single drivers. The phenotypic changes documented can be both a result of (1) population-level changes in the genetic pool (see above) or through (2) “nongenetic” responses of an individual (phenotypic plasticity). It should be noted that these two sources for population-level variation are not mutually exclusive. In fact, a genetic change can give rise to a change in phenotypic plasticity, and changes in phenotypic plasticity can lead to a new phenotype for natural and sexual selection to act upon, changing the genetic pool to the coming generations.
13.5.1 Physiology
13.5.1.1 Stress Physiology and Its Implications
The main physiological responses investigated in relation to urbanization or to single urban stressors is stress physiology (oxidative stress and corticosterone, commonly referred to as a stress hormone). Oxidative stress is the key target for toxicological research but also in relation to cost of life, since oxidative stress is part of the unavoidable aging process (Isaksson et al. 2011; Isaksson 2015). Environmental influences on oxidative stress can be multiple, e.g., pollution, radiation, disease, and food intake. However, the main factor in the urban environment is probably chemical pollution (such as NOx and soot, Fig. 13.1). Many of the urban air pollutants act as prooxidants, which will react with and cause damage to life-sustaining molecules such as proteins, lipids, and DNA, unless they are detoxified by the protective antioxidants. Oxidative damages are commonly used as biomarkers of poor health, leading to premature death. The first response to pollution or prooxidants is to increase the antioxidant responses, and this is also what birds, as well as humans, generally do in urban environments (Isaksson 2010, 2015; Salmón et al. 2018). However, the upregulation is not always sufficiently high to avoid oxidative damage and species’ as well as individuals’ capacity to deal with oxidative stress varies. For example, some sparrow species (Passeridae) have a poorer capacity to block generation of oxidative damages to proteins and lipids in the urban environment compared to the tit species (Paridae) living in the same urban environments (Isaksson et al. 2017; Salmón et al. 2018). Consequently, the physiological response and capacity vary across urban-dwelling species and, ultimately, the negative physiological effects related to urbanization.
Another aging biomarker that may be linked to oxidative stress is the shortening of telomeres (von Zglinicki 2002; Boonekamp et al. 2017). Telomeres are the outer protective ends of the chromosomes, which shorten throughout an individual’s life and can shorten more rapidly if exposed to stress such as irradiation, malnutrition, or pollution. When the telomeres reach a critical length, the cell cannot function, ultimately leading to cellular death. Early life in an urban environment has proven particularly challenging for Great Tits. In a cross-fostering experiment of 2-day-old chicks, half broods were swapped between an urban city park and a forest. Twelve days later, a blood sample was taken and analyzed for telomere length. The Great Tits that grew up in the urban habitat (independent of population origin) had significantly shorter telomeres than the chicks that grew up in the forest (Salmón et al. 2016). These individuals were followed to the next season, and it was clear that only the individuals with relatively long telomeres were recaptured the following breeding season, indicating that individuals with short telomeres had not survived the winter and this effect was significantly stronger in the urban environment (Salmón et al. 2017). This suggests that telomere length matters and that urban environmental stress significantly affects survival. To date, all studies on oxidative stress and telomeres are linked to urbanization and not to a specific urban driver; however, it is clear that regardless of source, the urban environment is challenging for birds and their physiological responses do not always circumvent the negative effects.
Another pathway to remove toxic heavy metals has been proposed for birds, namely, their incorporation into feathers. Melanin-pigmented feathers seem to incorporate more heavy metals, specifically zinc and lead, compared to feathers that are paler (non-melanin-pigmented). This was shown in pigeons of different color morphs which suggests that the dark melanin-pigmented Feral Pigeons could benefit in urban areas since they detoxify the blood stream from heavy metals, thereby reducing the potentially negative effect from pollution (Chatelain et al. 2014). Indeed, several studies have shown that the dark morph is more common in cities across Europe (Obukhova 2007; Jacquin et al. 2013).
Hormones have also been of great interest in relation to how birds respond to urbanization (Bonier 2012), especially stress and reproductive hormones. This is because hormones trigger behavioral and other physiological responses, thus representing key targets for selection. Changes in hormones have been associated with resource availability, conspecific interactions, predation, night light (see below), and human disturbance (Bonier 2012). Baseline levels of corticosterone seem to depend highly on sex, life-history stage, and/or species (Bonier 2012). Thus, studies on avian stress hormones have so far not been able to reveal any consistent pattern in relation to urbanization. Regarding hormones that affect reproduction, gonadotropin-releasing hormone is stimulated by day length. Due to the artificial night lighting in urban habitats the day becomes longer than in areas lacking street lights. Indeed, in urban environments gonadotropin-relasing hormone and other reproductive hormones are more stimulated which is the likely mechanistic explanation for the advancement of the timing of mating behaviors and reproduction (Deviche and Davies 2014).
13.5.1.2 Nutritional Physiology and Its Implications
Birds are provided with a great deal of anthropogenic food. This food can be either provided on bird feeders (e.g., peanuts, bread, sugar-water, sunflower seeds), or birds can scavenge from for example garbage bins or restaurant terraces. It is clear that many of the gregarious urban exploiter and invasive species take advantage of this resource (e.g., Robb et al. 2008; Galbraith et al. 2017). Food abundance and reliability change many phenotypic characters such as fat storage and flight-initiation distance, i.e., the tameness of the birds (Liker et al. 2008; Andersson et al. 2015; Møller et al. 2015). However, in relation to nutritional physiology, it is only recently that it has gained interest among ornithologists (e.g., Isaksson 2015). This goes hand in hand with human nutrition and the many negative health effects documented from our increased fat and sugar intake. Regarding fat intake, it is not only the increased consumption that is negative but also the changed composition of fatty acids, which affects, for example, inflammatory responses and metabolic rate. For example, in urban Great Tits there were less functionally important polyunsaturated fatty acids in yolks compared to yolks from eggs laid in the forest (Toledo et al. 2016). In addition, adult Great Tits show seasonal differences in fatty acid composition which reflect the differences in availability of anthropogenic food sources (Andersson et al. 2015). Furthermore and interestingly, the proportions of fatty acids were frequently in opposite directions when comparing species from the two families—Paridae and Passeridae. These patterns suggest that sparrows and tits feed on different food sources across the urban-rural gradient (Isaksson et al. 2017). Although the diet items were not quantified for fatty acids in any of the studies, certain polyunsaturated fatty acids are essential, i.e., they need to be obtained through the diet. The impact of these dietary differences shown in the birds’ physiology is still unknown, but given the large-scale feeding of birds, it screams for attention (see, e.g., Harrison et al. 2010; Plummer et al. 2013).
Dietary antioxidants have also received attention in relation to urbanization, especially carotenoids (Isaksson and Andersson 2007; Møller et al. 2010). Carotenoids are synthesized by plants; thus birds need to obtain carotenoids through their diet. During the breeding season, many passerines rely on caterpillars for raising their brood, and these leaf-eating caterpillars represent a rich source of carotenoids (Isaksson and Andersson 2007). In cities, caterpillars are generally of lower abundance due to the high pollution levels and lack of native tree species (e.g., Pollock et al. 2017; Isaksson unpublished). However, it has also been shown that urban trees of birch Betula sp. and oak Quercus sp. (native to Northern Europe) produce less carotenoids (Isaksson 2009), which affects the carotenoid concentration of caterpillars and, ultimately, the carotenoid availability for birds (Isaksson and Andersson 2007). Carotenoids are important nutrients for proper development, the immune system, night vision, and yellow-red plumage pigmentation. Lack of carotenoids has been shown to affect breeding success, through smaller clutch sizes and reduced fledging success (Blount et al. 2002; Ewen et al. 2009). Nutritional limitation for breeding females and developing chicks is probably one of the reasons for the often-lower breeding success in urban environments (e.g., Chamberlain et al. 2009; Charmantier et al. 2017; Meyrier et al. 2017; Pollock et al. 2017). Moreover, carotenoid pigmentation is often used as an indicator of individual quality (i.e., nutritional quality and/or immunocompetence) used during mate choice. Urban Great Tits and also Great Tits living close to a copper smelter have a paler yellow (carotenoid-based) plumage coloration compared to their rural conspecifics (Eeva et al. 1998; Isaksson et al. 2005; Fig. 13.5). A paler plumage coloration affects the males’ attraction potential (i.e., sexual signal value), and females may want or need to evaluate other characters, which may reduce female choice based on pigmentation and instead enhance the “sexiness” of other characters, which could lead to population divergence and reproductive isolation in the long run.
13.5.2 Behavior
13.5.2.1 Behavioral Responses to Chemical Pollution
Most responses documented to chemical pollution are physiological; however, also behavioral responses have been shown. In China, Li and colleagues documented the time it took for homing pigeons to find their way home. This race was conducted in an area with considerable air pollution, and it was shown that pigeons were homed faster when the air pollution level was especially high (Li et al. 2016). By doing this, the birds escape the high pollution levels, which can have negative effects on their performance and health. Another novel behavior is the use of cigarette butts in nests. Both House Sparrows and House Finches have been shown to include cigarette butts as nest materials. The nicotine appears to work as an effective insect repellent against ectoparasites and the more cigarette butts the less infested was the nest (Suárez-Rodríguez et al. 2013). However, this repellent seems to come with physiological costs to the parent birds which show increased genotoxic damage (Suárez-Rodríguez et al. 2017).
13.5.2.2 Behavioral Responses to Noise
The list of behavioral responses to noise is long and includes changes in, for example, (1) vocal communication, (2) avoidance responses, and (3) fight-flight responses (e.g., Ortega 2012; Nemeth et al. 2013; LaZerte et al. 2017). The key feature of urban background noise is the low frequency, hence masking songs in this frequency range. Thus, a shift to higher frequency songs should be favored in the city. This is exactly what has been found in Great Tits (among many other species) in noisy natural environments (e.g., Slabbekoorn and Peet 2003). The higher minimum frequency song of urban Great Tits could also be experimentally induced, suggesting a highly plastic response (Halfwerk and Slabbekoorn 2009). However, a recent study challenges that plasticity is the cause for song differences across noisy habitats (Zollinger et al. 2017). The study by Zollinger and colleagues found that Great Tits sang consistently on pitch and with the same mean minimum frequencies in all noise conditions. This suggests that the observed changes between urban and forest populations may not be the result of individuals’ plastic response, but instead be the outcome of slower, population-wide changes through selection (Zollinger et al. 2017). These population-level shifts in song could be driven by sexual selection, however, it could also be driven by body size and/or beak morphology (i.e., a smaller body and beak would lead to higher frequency songs). Urban environments have different food items available which repeatedly has been shown to affect beak morphology (e.g., Badyaev et al. 2008; Bosse et al. 2017). For example, urban House Finches were shown to feed on larger, harder foods than their counterparts in natural Sonoran Desert habitats (e.g., sunflower seeds versus cacti and grass seeds, respectively) (Badyaev et al. 2008). This led to a selection for larger bills in the urban population, which ultimately affected courtship song. This was suggested to give rise to a novel trade-off between bill size and song characteristics in urban environments. Possibly, these novel trade-offs between morphology and song in different environments could result in a nonoptimal song and mask the effect of noise on song.
Moreover, also species characters can influence the strength of vocal responses to urbanization. These species characters can, for example, be degree of vocal communication within species that use vocal communication to attract a mate, to defend a territory, or to warn for predators. Species also vary in their hearing capacity—some bird species hear certain frequencies and amplitudes better than other species, sometimes even within the ultrasonic range (Ortega 2012). Some species have solved the masking issue of their song and calls by changes in their daily rhythm. This is the case for European Robins Erithacus rubecula. The urban Robins reduce their acoustic interferences by singing during night, and the effect of daily noise was indeed a stronger driver of this change in behaviour than the night-light pollution through changed sleep patterns (see also below) (Fuller et al. 2007).
13.5.2.3 Behavioral Responses to ALAN
The effects on the navigation and orientation system of nocturnally migrating birds are the most well-known negative effects caused by ALAN. The migrating birds are attracted to urban ALAN, hence they appear more frequently in urban lit areas during autumn migration than during other seasons (La Sorte et al. 2017). Apart from the general ALAN, light installations are very popular nowadays; unfortunately, the light beams from installations can “trap” birds, i.e., birds are attracted to the beam and, while in the beam, they get disorientated and fly around in circles within the beam—they get trapped. This was shown for the light installation put up in New York as memorial tribute to the 9/11 victims. Over a billion birds were affected during a few days count repeated over multiple years (van Doren et al. 2017). Migrating birds were in 20 times higher densities in the light beams compared to the nearby surroundings. Nowadays, the city of New York turn of the light installations when the bird densities get too high within the beam. Another sensitive group for ALAN are seabird fledglings. During their first flight to the sea, they can get disorientated by ALAN and end up grounded at lit highways and roads (Rodriguez et al. 2014). By turning off road light during fledging it reduces the number of birds that ground on the road (dead or alive) (Rodriguez et al. 2014).
Reproductive timing and mating behaviors are also affected by ALAN (e.g., Kempenaers et al. 2010; Dominoni et al. 2013a). A study of city and forest Common Blackbirds revealed that when exposed to ALAN in captivity, the reproductive system developed one month earlier than in individuals that were kept with dark nights. However, even more interesting was the fact the bird that originated from the city responded stronger to ALAN treatment compared to the forest birds, i.e., they had an even earlier start than the forest birds (Dominoni et al. 2013b).
Furthermore, correlational studies of ALAN have for long suggested that birds start their dawn singing earlier in urban lit areas; however, recently a large-scale experiment using different light colors could not confirm this for the 14 species investigated (Da Silva et al. 2017). In another experimental study, Blue Tits responded to ALAN by advancing their daily activity onset and more so for red and white light than for green light (de Jong et al. 2017). Similarly, experimental lighting progressively advanced the dawn singing of Robins (Da Silva et al. 2016). Thus, at least for some bird species, urban influences through ALAN can be mitigated by changing the spectral characteristics and intensity of outdoor lighting.
Another concern with ALAN is the effect it might have on sleep. Anyone who has tried to sleep with the lights on knows how disruptive that can be. The sleep hormone, melatonin, is affected by light and a decline in melatonin with ALAN has been shown in Great Tits and Blackbirds (Dominoni et al. 2013a; de Jong et al. 2016) and female Great Tits spend a greater proportion of the night awake (Raap et al. 2015).