Increased Noise Levels Have Different Impacts on the Anti-Predator Behaviour of Two Sympatric Fish Species

Animals must avoid predation to survive and reproduce, and there is increasing evidence that man-made (anthropogenic) factors can influence predator−prey relationships. Anthropogenic noise has been shown to have a variety of effects on many species, but work investigating the impact on anti-predator behaviour is rare. In this laboratory study, we examined how additional noise (playback of field recordings of a ship passing through a harbour), compared with control conditions (playback of recordings from the same harbours without ship noise), affected responses to a visual predatory stimulus. We compared the anti-predator behaviour of two sympatric fish species, the three-spined stickleback (Gasterosteus aculeatus) and the European minnow (Phoxinus phoxinus), which share similar feeding and predator ecologies, but differ in their body armour. Effects of additional-noise playbacks differed between species: sticklebacks responded significantly more quickly to the visual predatory stimulus during additional-noise playbacks than during control conditions, while minnows exhibited no significant change in their response latency. Our results suggest that elevated noise levels have the potential to affect anti-predator behaviour of different species in different ways. Future field-based experiments are needed to confirm whether this effect and the interspecific difference exist in relation to real-world noise sources, and to determine survival and population consequences.     

Experimental evidence for an impact of anthropogenic noise on dawn chorus timing in urban birds

Many animal species are living in urban areas, where they encounter human‐altered environmental conditions. Artificial light and traffic noise are two of the most prominent anthropogenic factors, both of which potentially affect animal life. Here we studied the changes in traffic noise conditions over the morning in the urban bird habitat of the city of Seville, Spain. We tested experimentally whether noise from human activities can cause a shift in the timing of birdsong activity. Our data revealed that noise conditions vary markedly among our replicate set of twelve streets. Relatively quiet streets show low base‐line amplitude levels early in the morning, with frequent events of brief noise bursts, followed by a strong rise in noise levels. Relatively noisy streets have high base‐line amplitude levels from a much earlier start in the morning. Experimental exposure data revealed a noise‐related earlier start of dawn singing for two out of six species: the spotless starling Sturnus unicolor and the house sparrow Passer domesticus. Our experiment did not cover earlier singing species and revealed no impact for species with more‐variable starting times of the dawn singing. Our study provides more insight into the intertwinings of bird and human behavior and confirms the potential for experimental approaches to successfully tackle questions related to the impact of anthropogenic factors on animal life in cities.     

How do anthropogenic contaminants (ACs) affect behaviour? Multi-level analysis of the effects of copper on boldness in hermit crabs

Natural animal populations are increasingly exposed to human impacts on the environment, which could have consequences for their behaviour. Among these impacts is exposure to anthropogenic contaminants. Any environmental variable that influences internal state could impact behaviour across a number of levels: at the sample mean, at the level of among-individual differences in behaviour (‘animal personality’) and at the level of within-individual variation in behaviour (intra-individual variation, ‘IIV’). Here we examined the effect of exposure to seawater-borne copper on the startle response behaviour of European hermit crabs, Pagurus bernhardus across these levels. Copper exposure rapidly led to longer startle responses on average, but did not lead to any change in repeatability indicating that individual differences were present and equally consistent in the presence and absence of copper. There was no strong evidence that copper exposure led to changes in IIV. Our data show that exposure to copper for 1 week produces sample mean level changes in the behaviour of hermit crabs. However, there is no evidence that this exposure led to changes in repeatability through feedback loops.     

URBAN NOISE PREDICTS SONG FREQUENCY IN NORTHERN CARDINALS AND AMERICAN ROBINS

ABSTRACT

We examined the extent to which acoustic noise in urban environments influences song characteristics and singing behaviour of Northern Cardinals Cardinalis cardinalis and American Robins Turdus migratorius. We predicted that, in response to loud noise, birds would improve signal transmission by (1) increasing singing rate and (2) adjusting song characteristics such as pitch and length. From May—July 2006, 42 cardinals and 53 robins were recorded in forests located within four acoustic environments in central Ohio: rural, residential, commercial, and highway. Following each recording, we measured ambient noise level and recorded information describing location, weather, habitat, and conspecific presence within 75 m. As predicted, frequency range was positively correlated with noise level for both species, but neither song length nor rate was related to noise level for either species. These data support the idea that anthropogenic noise influences avian singing behaviour and acts as a selective force in urban areas.     

A Test of the Effect of Male Song on Female Nesting Behaviour in the Serin (Serinus serinus): a Field Playback Experiment

It is well established, through laboratory experiments, that male song in birds can stimulate female reproductive activity, affecting their behaviour and physiology, such as follicular growth, nest building and egg‐laying. However no clear demonstration has yet been provided that this effect works under natural conditions. Previous work in natural populations of serins showed that female nest‐building behaviour correlated with male singing time. Furthermore male serin song peaked exactly in the day that rapid follicular growth was estimated to start in females, suggesting that in this species song may also serve to stimulate the female's reproductive development. Direct causal evidence, however, was lacking. We conducted field playback experiments to investigate how song can influence female nesting activity during nest building. Our results show that females who listened daily to playbacks of serin songs, during the nest‐building stage, spent more time nest building than females that were not exposed to additional songs. Moreover, the singing behaviour of the mated males was not affected by the playbacks, suggesting that the song playback treatment had a direct positive effect on female nesting behaviour.     

Individual‐ and population‐level personalities in a floriphilic katydid

Behaviour, including personality, informs us about the response of animals towards their changing environment. Despite the widespread occurrence of florivorous insects and the important but often underrated ecological roles that they play, the study of florivore behaviour is neglected relative to that of pollinators and other herbivores. Specifically, we do not know how different personality types can develop among florivores and enable them to persist in habitats with an ephemeral and dynamic availability of food resources. To address this knowledge gap, we investigated the following questions: whether the (a) inter‐individual differences of exploration and boldness are consistent; (b) inter‐population differences of exploration and boldness are consistent; (c) exploration and boldness are correlated. We collected individuals of the polyphagous floriphilic katydid, Phaneroptera brevis from four populations from wasteland sites in Singapore and performed a personality assay conducted in an insectary to investigate the exploratory and boldness levels of the individuals and populations. The major novel finding was that the floriphilic P. brevis katydids exhibit population‐level personality types for boldness, but not for exploration. Some katydid individuals were consistently more exploratory and bolder than other individuals. However, contrary to our predictions, we did not find any evidence of behavioural syndromes in the katydid individuals, as the boldness level for individuals was not significantly correlated with exploration for individuals. This suggests that an individual which is more exploratory may not be equally keen to take risks and consume novel food that it encounters. Our findings also suggest that boldness and exploration are linked to ecologically important behaviours, but more studies are needed to better understand population‐level personality and how and why natural selection may favour the evolution of personality in certain populations.     

Hierarchical Levels of Seed Predation Variation by Introduced Beetles on an Endemic Mediterranean Palm

Seed predators can limit plant recruitment and thus profoundly impinge the dynamics of plant populations, especially when diverse seed predators (e.g., native and introduced) attack particular plant populations. Surprisingly, however, we know little concerning the potential hierarchy of spatial scales (e.g., region, population, patch) and coupled ecological correlates governing variation in the overall impact that native and introduced seed predators have on plant populations. We investigated several spatial scales and ecological correlates of pre-dispersal seed predation by invasive borer beetles in Chamaerops humilis (Arecaceae), a charismatic endemic palm of the Mediteranean basin. To this end, we considered 13 palm populations (115 palms) within four geographical regions of the Iberian Peninsula. The observed interregional differences in percentages of seed predation by invasive beetles were not significant likely because of considerable variation among populations within regions. Among population variation in seed predation was largely related to level of human impact. In general, levels of seed predation were several folds higher in human-altered populations than in natural populations. Within populations, seed predation declined significantly with the increase in amount of persisting fruit pulp, which acted as a barrier against seed predators. Our results revealed that a native species (a palm) is affected by the introduction of related species because of the concurrent introduction of seed predators that feed on both the introduced and native palms. We also show how the impact of invasive seed predators on plants can vary across a hierarchy of levels ranging from variation among individuals within local populations to large scale regional divergences.     

The song of Skylarks Alauda arvensis indicates the deterioration of an acoustic environment resulting from wind farm start‐up

The rapid development of wind energy may have negative effects on bird populations, including collisions with turbines, displacement due to disturbance or habitat loss, indirect effects of reduced breeding success and barrier effects. This challenging conservation issue has attracted a great deal of interest, but the noise generated by turbines has been largely overlooked. Here, we studied acoustic behaviour of Skylarks Alauda arvensis in relation to wind farm start‐up to assess whether a change in song parameters can indicate a deterioration in the acoustic environment. We recorded territorial males displaying close to operating and non‐operating turbines and at a control site without turbines. In the following breeding season, we undertook replications at the same sites, except that the non‐operating turbines were now in operation. We found that Skylarks displaying at the wind farm were affected by wind turbine noise. Males singing close to operating wind turbines sang higher‐frequency songs than males from a control site and those that displayed near non‐operating turbines. In addition, an upward frequency shift in songs was observed when non‐operating turbines started to operate in the consecutive season. We therefore conclude that the frequency shift observed did not result from turbine presence, but from the noise they started to generate. This shows that a change in song parameters may reliably and within a relatively short time indicate a significant deterioration of the acoustic environment as a consequence of wind farm start‐up. This may help conservation biologists to identify species and populations that are particularly susceptible to wind farm noise.     

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

The effect of neighbours and females on dawn and daytime singing behaviours by male chipping sparrows

Bird song may play an important role for communication among territorial neighbours, but the effect of neighbours on song use is still not well known. My previous field observations suggested that male chipping sparrows, Spizella passerina, use the dawn chorus for interactions among neighbouring males, and use day song for female attraction. To determine how these social factors may influence dawn and daytime singing behaviour, I conducted a series of experiments in which I removed the male neighbours or the female mate of territorial males during 1998-2000. Following removal of all neighbouring males, the solitary male either stopped or reduced his dawn chorus (N=9), but did not change his daytime singing behaviour. After one of the neighbouring males was returned to his territory, the focal male resumed and increased his dawn bout, accompanied with close-range countersinging. Following the removal of a territorial male's mate, the widowed male did not change the dawn chorus, but significantly increased his day song. This study thus revealed that, in chipping sparrows, the presence or absence of neighbouring males has a significant effect on the dawn chorus singing behaviour of territorial males. The presence or absence of a male's mate, in contrast, has a strong influence on a male's daytime singing behaviour. This study also supports the hypothesis that the dawn chorus and daytime song have different functions.     

Metabolic and respiratory costs of increasing song amplitude in zebra finches

Bird song is a widely used model in the study of animal communication and sexual selection, and several song features have been shown to reflect the quality of the singer. Recent studies have demonstrated that song amplitude may be an honest signal of current condition in males and that females prefer high amplitude songs. In addition, birds raise the amplitude of their songs to communicate in noisy environments. Although it is generally assumed that louder song should be more costly to produce, there has been little empirical evidence to support this assumption. We tested the assumption by measuring oxygen consumption and respiratory patterns in adult male zebra finches (Taeniopygia guttata) singing at different amplitudes in different background noise conditions. As background noise levels increased, birds significantly increased the sound pressure level of their songs. We found that louder songs required significantly greater subsyringeal air sac pressure than quieter songs. Though increased pressure is probably achieved by increasing respiratory muscle activity, these increases did not correlate with measurable increases in oxygen consumption. In addition, we found that oxygen consumption increased in higher background noise, independent of singing behaviour. This observation supports previous research in mammals showing that high levels of environmental noise can induce physiological stress responses. While our study did not find that increasing vocal amplitude increased metabolic costs, further research is needed to determine whether there are other non-metabolic costs of singing louder or costs associated with chronic noise exposure.     

Facing the Heat: Does Desiccation and Thermal Stress Explain Patterns of Orientation in an Intertidal Invertebrate?

A key challenge for ecologists is to quantify, explain and predict the ecology and behaviour of animals from knowledge of their basic physiology. Compared to our knowledge of many other types of distribution and behaviour, and how these are linked to individual function, we have a poor level of understanding of the causal basis for orientation behaviours. Most explanations for patterns of animal orientation assume that animals will modify their exposure to environmental factors by altering their orientation. We used a keystone grazer on rocky shores, the limpet Cellana tramoserica, to test this idea. Manipulative experiments were done to evaluate whether orientation during emersion affected limpet desiccation or body temperature. Body temperature was determined from infrared thermography, a technique that minimises disturbance to the test organism. No causal relationships were found between orientation and (i) level of desiccation and (ii) their body temperature. These results add to the growing knowledge that responses to desiccation and thermal stress may be less important in modifying the behaviour of intertidal organisms than previously supposed and that thermoregulation does not always reflect patterns of animal orientation. Much of what we understand about orientation comes from studies of animals able to modify orientation over very short time scales. Our data suggests that for animals whose location is less flexible, orientation decisions may have less to do with responses to environmental factors and more to do with structural habitat properties or intrinsic individual attributes. Therefore we suggest future studies into processes affecting orientation must include organisms with differing levels of behavioural plasticity.     

Impacts of regular and random noise on the behaviour,growth and development of larval Atlantic cod (Gadus morhua)

Anthropogenic noise impacts behaviour and physiology in many species, but responses could change with repeat exposures. As repeat exposures can vary in regularity, identifying regimes with less impact is important for regulation. We use a 16-day split-brood experiment to compare effects of regular and random acoustic noise (playbacks of recordings of ships), relative to ambient-noise controls, on behaviour, growth and development of larval Atlantic cod (Gadus morhua). Short-term noise caused startle responses in newly hatched fish, irrespective of rearing noise. Two days of both regular and random noise regimes reduced growth, while regular noise led to faster yolk sac use. After 16 days, growth in all three sound treatments converged, although fish exposed to regular noise had lower body width–length ratios. Larvae with lower body width–length ratios were easier to catch in a predator-avoidance experiment. Our results demonstrate that the timing of acoustic disturbances can impact survival-related measures during development. Much current work focuses on sound levels, but future studies should consider the role of noise regularity and its importance for noise management and mitigation measures.     

Population,Behavioural and Physiological Responses of an Urban Population of Black Swans to an Intense Annual Noise Event

Wild animals in urban environments are exposed to a broad range of human activities that have the potential to disturb their life history and behaviour. Wildlife responses to disturbance can range from emigration to modified behaviour, or elevated stress, but these responses are rarely evaluated in concert. We simultaneously examined population, behavioural and hormonal responses of an urban population of black swans Cygnus atratus before, during and after an annual disturbance event involving large crowds and intense noise, the Australian Formula One Grand Prix. Black swan population numbers were lowest one week before the event and rose gradually over the course of the study, peaking after the event, suggesting that the disturbance does not trigger mass emigration. We also found no difference in the proportion of time spent on key behaviours such as locomotion, foraging, resting or self-maintenance over the course of the study. However, basal and capture stress-induced corticosterone levels showed significant variation, consistent with a modest physiological response. Basal plasma corticosterone levels were highest before the event and decreased over the course of the study. Capture-induced stress levels peaked during the Grand Prix and then also declined over the remainder of the study. Our results suggest that even intensely noisy and apparently disruptive events may have relatively low measurable short-term impact on population numbers, behaviour or physiology in urban populations with apparently high tolerance to anthropogenic disturbance. Nevertheless, the potential long-term impact of such disturbance on reproductive success, individual fitness and population health will need to be carefully evaluated.     

Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp. lusitanicum

Nectar robbery is usually thought to impact negatively on the reproductive success of plants, but also neutral or even positive effects have been reported. Very few studies have investigated the effects of nectar robbing on the behaviour of legitimate pollinators so far. Such behavioural changes may lead to the reduction of geitonogamy or to increased pollen movement. We simulated nectar robbing in experimental sites as well as in natural populations of Aconitum napellus ssp. lusitanicum, a rare plant pollinated by long-tongued bumblebees. In an experimental setup, we removed the nectaries of 40 % of the flowers, which is similar to rates of robbing observed in wild populations. Patches of plants with experimentally robbed flowers were compared with control patches containing plants with untreated flowers. We observed pollinator behaviour, mimicked male reproductive success (pollen dispersal) using fluorescent dye, and measured female reproductive success (seed set). The main legitimate visitors were bumblebees while honeybees were often observed robbing nectar. They did so by “base working”, i.e. sliding between tepals. Bumblebees tended to visit fewer flowers per plant and spent less time per single flower when these had been experimentally robbed. This change in behaviour consequently increased the proportion of flowers visited by bumblebees in patches with robbed flowers. Fluorescent dye mimicking pollen flow was dispersed larger distances after pollinators had visited patches with robbed flowers compared to control patches. Average seed set per plant was not affected by nectar robbing. Our results demonstrated that A. napellus does not suffer from nectar robbery but may rather benefit via improved pollen dispersal and thus, male reproductive success. Knowledge on such combined effects of behavioural changes of pollinators due to nectar robbery is important to understand the evolutionary significance of exploiters of such mutualistic relationships between plants and their pollinators.     

Constitutive versus responsive gene expression strategies for growth in changing environments

Microbes respond to changing environments by adjusting gene expression levels to the demand for the corresponding proteins. Adjusting protein levels is slow, consequently cells may reach the optimal protein level only by a time when the demand changed again. It is therefore not a priori clear whether expression “on demand” is always the optimal strategy. Indeed, many genes are constitutively expressed at intermediate levels, which represents a permanent cost but provides an immediate benefit when the protein is needed. Which are the conditions that select for a responsive or a constitutive expression strategy, what determines the optimal constitutive expression level in a changing environment, and how is the fitness of the two strategies affected by gene expression noise? Based on an established model of the lac- and gal-operon expression dynamics, we study the fitness of a constitutive and a responsive expression strategy in time-varying environments. We find that the optimal constitutive expression level differs from the average demand for the gene product and from the average optimal expression level; depending on the shape of the growth rate function, the optimal expression level either provides intermediate fitness in all environments, or maximizes fitness in only one of them. We find that constitutive expression can provide higher fitness than responsive expression even when regulatory machinery comes at no cost, and we determine the minimal response rate necessary for “expression on demand” to confer a benefit. Environmental and inter-cellular noise favor the responsive strategy while reducing fitness of the constitutive one. Our results show the interplay between the demand-frequency for a gene product, the genetic response rate, and the fitness, and address important questions on the evolution of gene regulation. Some of our predictions agree with recent yeast high throughput data, for others we propose the experiments that are needed to verify them.     

Female conspecifics restore rhythmic singing behaviour in arrhythmic male zebra finches

The present study investigated whether pairing with a conspecific female would restore rhythmicity in the singing behaviour of arrhythmic male songbirds. We recorded the singing and, as the circadian response indicator, monitored the activity–rest pattern in male zebra finches (Taeniopygia guttata) housed without or with a conspecific female under 12 h light: 12 h darkness (12L:12D) or constant bright light (LL_bright). Both unpaired and paired birds exhibited a significant daily rhythm in the singing and activity behaviour, but paired birds, under 12L:12D, showed a ~2 h extension in the evening. Exposure to LL_bright decayed rhythmicity, but the female presence restored rhythmic patterns without affecting the 24 h song output. In the acoustic features, we found a significant difference in the motif duration between unpaired and paired male songs. Overall, these results demonstrated for the first time the role of the female in restoring the circadian phenotype of singing behaviour in male songbirds with disrupted circadian functions, although how interaction between sexes affects the circadian timing of male singing is not understood yet. It is suggested that social cues rendered by a conspecific female could improve the circadian performance by restoring rhythmicity in the biological functions of the cohabiting arrhythmic male partner.     

Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.     

Passerine birds breeding under chronic noise experience reduced fitness

Background

Fitness in birds has been shown to be negatively associated with anthropogenic noise, but the underlying mechanisms remain obscure. It is however crucial to understand the mechanisms of how urban noise impinges on fitness to obtain a better understanding of the role of chronic noise in urban ecology. Here, we examine three hypotheses on how noise might reduce reproductive output in passerine birds: (H1) by impairing mate choice, (H2) by reducing territory quality and (H3) by impeding chick development.

Methodology/Principal Findings

We used long-term data from an island population of house sparrows, Passer domesticus, in which we can precisely estimate fitness. We found that nests in an area affected by the noise from large generators produced fewer young, of lower body mass, and fewer recruits, even when we corrected statistically for parental genetic quality using a cross-fostering set-up, supporting H3. Also, individual females provided their young with food less often when they bred in the noisy area compared to breeding attempts by the same females elsewhere. Furthermore, we show that females reacted flexibly to increased noise levels by adjusting their provisioning rate in the short term, which suggests that noise may be a causal factor that reduces reproductive output. We rejected H1 and H2 because nestbox occupancy, parental body mass, age and reproductive investment did not differ significantly between noisy and quiet areas.

Conclusions/Significance

Our results suggest a previously undescribed mechanism to explain how environmental noise can reduce fitness in passerine birds: by acoustically masking parent–offspring communication. More importantly, using a cross-fostering set-up, our results demonstrate that birds breeding in a noisy environment experience significant fitness costs. Chronic noise is omnipresent around human habitation and may produces similar fitness consequences in a wide range of urban bird species.