Noise and light pollution elicit endocrine responses in urban but not forest frogs.

Urban areas are characterised by the presence of sensory pollutants, such as anthropogenic noise and artificial light at night (ALAN). Animals can quickly adapt to novel environmental conditions by adjusting their behaviour, which is proximately regulated by endocrine systems. While endocrine responses to sensory pollution have been widely reported, this has not often been linked to changes in behaviour, hampering the understanding of adaptiveness of endocrine responses. Our aim was, therefore, to investigate the effects of urbanisation, specifically urban noise and light pollution, on hormone levels in male urban and forest túngara frogs (Engystomops pustulosus), a species with reported population divergence in behaviour in response to urbanisation. We quantified testosterone and corticosterone release rates in the field and in the lab before and after exposure to urban noise and/or light. We show that urban and forest frogs differ in their endocrine phenotypes under field as well as lab conditions. Moreover, in urban frogs exposure to urban noise and light led, respectively, to an increase in testosterone and decrease in corticosterone, whereas in forest frogs sensory pollutants did not elicit any endocrine response. Our results show that urbanisation, specifically noise and light pollution, can modulate hormone levels in urban and forest populations differentially. The observed endocrine responses are consistent with the observed behavioural changes in urban frogs, providing a proximate explanation for the presumably adaptive behavioural changes in response to urbanisation.

Anthropogenic noise and light alter temporal but not spatial breeding behavior in a wild frog.

Increasing urbanization has led to large-scale land-use changes, exposing persistent populations to drastically altered environments. Sensory pollutants, including low-frequency anthropogenic noise and artificial light at night (ALAN), are typically associated with urban environments and known to impact animal populations in a variety of ways. Both ALAN and anthropogenic noise can alter behavioral and physiological processes important for survival and reproduction, including communication and circadian rhythms. Although noise and light pollution typically co-occur in urbanized areas, few studies have addressed their combined impact on species' behavior. Here, we assessed how anthropogenic noise and ALAN can influence spatial and temporal variation in breeding activity of a wild frog population. By exposing artificial breeding sites inside a tropical rainforest to multiple sensory environments, we found that both anthropogenic noise and ALAN impact breeding behavior of túngara frogs (Engystomops pustulosus), albeit in different ways. Males arrived later in the night at their breeding sites in response to anthropogenic noise. ALAN, on the other hand, led to an increase in calling effort. We found no evidence that noise or light pollution either attracted frogs to or repelled frogs from breeding sites. Thus, anthropogenic noise may negatively affect calling males by shifting the timing of sexual signaling. Conversely, ALAN may increase the attractiveness of calling males. These changes in breeding behavior highlight the complex ways that urban multisensory pollution can influence behavior and suggest that such changes may have important ecological implications for the wildlife that are becoming increasingly exposed to urban multisensory pollution.

A comprehensive overview of the effects of urbanisation on sexual selection and sexual traits.

Urbanisation can affect mating opportunities and thereby alter inter- and intra-sexual selection pressures on sexual traits. Biotic and abiotic urban conditions can influence an individual's success in pre- and post-copulatory mating, for example through impacts on mate attraction and mate preference, fertilisation success, resource competition or rival interactions. Divergent sexual selection pressures can lead to differences in behavioural, physiological, morphological or life-history traits between urban and non-urban populations, ultimately driving adaptation and speciation. Most studies on urban sexual selection and mating interactions report differences between urban and non-urban populations or correlations between sexual traits and factors associated with increased urbanisation, such as pollution, food availability and risk of predation and parasitism. Here we review the literature on sexual selection and sexual traits in relation to urbanisation or urban-associated conditions. We provide an extensive list of abiotic and biotic factors that can influence processes involved in mating interactions, such as signal production and transmission, mate choice and mating opportunities. We discuss all relevant data through the lens of two, non-mutually exclusive theories on sexual selection, namely indicator and sensory models. Where possible, we indicate whether these models provide the same or different predictions regarding urban-adapted sexual signals and describe different experimental designs that can be useful for the different models as well as to investigate the drivers of sexual selection. We argue that we lack a good understanding of: (i) the factors driving urban sexual selection; (ii) whether reported changes in traits result in adaptive benefits; and (iii) whether these changes reflect a short-term ecological, or long-term evolutionary response. We highlight that urbanisation provides a unique opportunity to study the process and outcomes of sexual selection, but that this requires a highly integrative approach combining experimental and observational work.

Multisensory pollution: Artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major).

Urbanisation is increasing globally at a rapid pace. Consequently, wild species face novel environmental stressors associated with urban sprawl, such as artificial light at night and noise. These stressors have pervasive effects on the behaviour and physiology of many species. Most studies have singled out the impact of just one of these stressors, while in the real world they are likely to co-occur both temporally and spatially, and we thus lack a clear understanding of the combined effect of anthropogenic stressors on wild species. Here, we experimentally exposed captive male great tits (Parus major) to artificial light at night and 24 h noise in a fully factorial experiment. We then measured the effect of both these stressors on their own and their combination on the amount and timing of activity patterns. We found that both light and noise affected activity patterns when presented alone, but in opposite ways: light increased activity, particularly at night, while noise reduced it, particularly during the day. When the two stressors were combined, we found a synergistic effect on the total activity and the nighttime activity, but an antagonistic effect on daytime activity. The significant interaction between noise and light treatment also differed among forest and city birds. Indeed, we detected a significant interactive effect on light and noise on daytime, nighttime, dusktime and offset of activity of urban birds, but not of forest birds. These results suggest that both artificial light at night and anthropogenic noise can drive changes in activity patterns, but that the specific impacts depend on the habitat of origin. Furthermore, our results demonstrate that co-occurring exposure to noise and light can lead to a stronger impact at night than predicted from the additive effects and thus that multisensory pollution may be a considerable threat for wildlife.

Environmental conditions limit attractiveness of a complex sexual signal in the túngara frog.

Animals choosing particular display sites often balance sexual and natural selection pressures. Here we assess how physical properties of display sites can alter this balance by influencing signal production and attractiveness of the túngara frog (Physalaemus pustulosus). Males that call from very shallow water bodies (few mm depth) benefit from reduced predation risk, but by manipulating water levels, we show that this comes at a cost of reduced attractiveness to females. Our data show that calling from shallower water reduces a male's ability to float, limits the inflation of his vocal sac, and consequently reduces signal conspicuousness in terms of amplitude and complexity. Our results demonstrate that display site properties can set limits on signal production and attractiveness and may hence influence signal evolution. Signallers may shift between sites or engineer their display location, which can play a crucial role in signal divergence and speciation, particularly in a rapidly changing world.