Abstract
Anthropogenic noise is a major pollutant in terrestrial and aquatic ecosystems. Since the industrial revolution, human activities have become increasingly noisy, leading to both acute and chronic disturbance of a wide variety of animals. Chronic noise exposure can affect animals over their lifespan, leading to changes in species interactions and likely altering communities. However, the community-level impacts of chronic noise are not well-understood, which impairs our ability for effective mitigation. In this review, we address the effects of chronic noise exposure on communities and explore possible mechanisms underlying these effects. The limited studies on this topic suggest that noise can affect communities by changing the behavior and/or physiology of species in a community, which results in direct or knock-on consequences for other species in the ecosystem. Major knowledge gaps remain due to the logistically complex and financially expensive nature of the long-term studies needed to address these questions. By identifying these gaps and suggesting approaches to answer them, we provide a road map toward mitigating the effects of a noisy world.
1. Chronic noise can change communities
1.1. Introduction
Anthropogenic noise is recognized as a major global pollutant that has considerable implications for human health (; ; ) and the behavior, physiology and fitness of wildlife (). Indeed, a substantial body of research has been published over the past two decades that has explored the effects of noise pollution on animals across terrestrial and aquatic ecosystems (Shannon et al., 2016b; Sordello et al., 2020; ; ). Anthropogenic noise that significantly alters the acoustic environment has increased markedly since the Industrial Revolution both in terms of the level of sound exposure and geographical extent. The rise in noise pollution has been driven by population growth, mechanization, infrastructure development and increasing demand for resources (). For example, in the US continent-wide changes in the soundscape extend well beyond the boundaries of urban environments (), with 63% of protected areas experiencing sound exposure double that of the ambient level (). As such, noise has the potential to be a major selective force that can restructure wildlife communities (Swaddle et al., 2015). At the same time, noise does not persist long-term in the environment like many other pollutants—as was evidenced during the COVID-19 pandemic when lockdown measures led to sustained global quieting ()—which can facilitate mitigation measures and the reestablishment of natural soundscapes. The latency of recovery following noise removal will depend on the specific behavioral and/or physiological mechanisms that restructure wildlife communities, as well as the flexibility of species to adapt to the return of a more natural acoustic environment.
Field-based studies and laboratory experiments have provided considerable evidence that exposure to noise can cause a wide range of ecological impacts to wildlife (Shannon et al., 2016b; ; ). These include changing spatial distribution and deterring wildlife from important feeding and breeding areas, or interfering with crucial biological functions such as foraging performance (more food handling errors and discrimination errors), predator avoidance, prey detection and conspecific communication. Furthermore, there are direct physiological costs associated with exposure to noise from reduced sleep () to increasing stress hormone levels (Troïanowski et al., 2017). These varied impacts may lead to negative consequences for individual fitness, population levels and community structure (Slabbekoorn et al., 2010; ). Similarly, human communities experience physiological and behavioral effects from noise exposure that include sleep deprivation, cognitive impairment, elevated stress and annoyance, and a higher incidence of cardiovascular disease (Stansfeld and Matheson, 2003; Szalma and Hancock, 2011; ).
The behavioral effects of noise exposure are driven by four key mechanisms that are not mutually exclusive: (1) Noise masks critical sounds including communication of conspecifics and other relevant cues such as approaching danger; (2) noise distracts animals from attending to pertinent information in the environment; (3) noise is perceived as a direct threat, thereby altering behavioral responses of the animal; and/or (4) noise initiates chronic stress, leading to long-term behavioral and physiological changes in the animal. It is important to note that each of these mechanisms is capable of driving a change in animal distribution and habitat use, which can alter the composition and interaction of species at the community-level.
1.2. Chronic noise exposure
Although there have been considerable advances in our understanding of the biological responses associated with anthropogenic noise exposure over the past two decades, most are based on comparatively short-term experiments and observations (Shannon et al., 2016b; ). In addition, these studies have predominantly focused on a single species. However, transport networks, industry and urban environments are major sources of chronic anthropogenic noise that permeate natural and human transformed environments over the long-term. These noise sources are also characterized by acoustic energy mainly being concentrated in the low-frequency spectrum (<2 kHz), which travel further than high-frequency sounds and therefore potentially impact a wide range of species simultaneously.
Sound in nature is a complex and challenging physical phenomenon to measure, as it varies in terms of duration, frequency and amplitude. The acoustic characteristics of a given noise source and the perceptual capabilities (e.g., hearing sensitivity) of the species exposed to it will be instrumental in determining whether it is likely to significantly impact animal behavior and physiology (). Indeed, the duration, spectral and temporal characteristics of chronic noise may ultimately be as important as the amplitude when it comes to mediating long-term effects on animal communities. It is therefore crucial that scientists and wildlife practitioners accurately measure and report the specific sound characteristics of the noise source, as this information is critical for comparing research findings and understanding the specific levels of exposure that can drive a biological response (). Currently, many of the noise metrics used in research and monitoring are focused on human perceptual abilities, rather than considering the varied hearing thresholds of animal communities.
To fully understand the impacts of chronic anthropogenic noise exposure on animal communities it is necessary to conduct long-term studies (). These need to consider the effects of chronic exposure and lasting impacts after exposure has ended. However, a definition of chronic exposure is rarely given () and short-term and chronic exposure are on a continuum, making it difficult to classify exposure events in the field. For example, repeated short bursts of exposure (e.g., sonar) over longer periods (a few times a year for years) differ from medium-term exposure (continuous for weeks, e.g., construction site) in their effects. Additionally, what is considered chronic will also depend on the lifespan of the organism, which ranges from weeks to decades (). Construction of a gas pipeline that takes a year would thus be multi-generation exposure for some animals, whilst only a brief exposure for others. Finally, the effects of chronic exposure are expected to impact multiple species in the community, and should therefore be long enough to affect species with varying lifespans. Chronic noise exposure can thus have a low or high duty cycle, as long as it occurs regularly or long enough to impact species with varying lifespans. Therefore, we suggest a rather broad, but practical chronic exposure definition: “Exposure throughout a significant part of the lifespan of an animal, at regular enough intervals to have the potential of lasting impacts from the individual- to community-scale.”
1.3. State of the knowledge about chronic noise effects on communities
We conducted a search of peer-reviewed journal articles that have been published since 1970 and have addressed the effects of noise on animal communities. Our article search used the datasets provided in four previous systematic review papers (Shannon et al., 2016b; Sordello et al., 2020; ; ), as well as using the Web of Science and Google Scholar search engines to identify any further papers that were omitted from the reviews or that have been published in the last 2 years. The search terms we used were “anthropogenic,” “noise,” “wildlife,” “animal,” and “community.” We specifically focused on studies that explored whether noise exposure affected community-level composition (e.g., changes in abundance and diversity of multiple species) over time. The dataset comprised 48 papers published between 1995 and 2021 (Table 1 and Supplementary Material 1), of which 16 were not included in the previous review papers. Overall, the most common method to explore the community effects of noise was through direct observation (n = 29) followed by playback (n = 10) and natural experiment (n = 9). Seventy-nine percent of the studies (n = 38) reported negative effects of noise exposure in one taxonomic group (decreased abundance/species richness, decreased nesting, and decreased offspring survival/hatching success) while only one study documented a positive effect (increased abundance/species richness). The remainder revealed either no effect (n = 7) or mixed effects within the same taxonomic group (n = 7), with the direction depending upon the species. Birds featured in 38 (79%) of the studies; mammals, amphibians, reptiles and invertebrates were the least represented, featuring in one study each. Seventy-nine percent of the studies were conducted in either North America or Europe (n = 38). Seventy-one percent of the studies (n = 34) explored whether noise influenced abundance and/or species diversity.
TABLE 1
| Taxonomic group | ||||||||||||||||||||||||
| Plants | Worms | Arthropods | Fish | Amphibians | Reptiles | Birds | Mammals | |||||||||||||||||
| Effect | N | 0 | P | N | 0 | P | N | 0 | P | N | 0 | P | N | 0 | P | N | 0 | P | N | 0 | P | N | 0 | P |
| Negative | 1 | 1* | 1 | 1 | 1† | 2 | 1 | 1° | 3° | 18‡ | 7† | 1° | ||||||||||||
| Positive | 1 | |||||||||||||||||||||||
| Neutral | 1 | 1‡ | 1 | 4 | ||||||||||||||||||||
| Mixed | 1 | 1* | 1 | 2 | 1 | 1 | ||||||||||||||||||
Number of studies in the literature review (S2) that investigated the effects of noise on communities separated by taxonomic group.
N, natural experiment; O, observational; P, playback experiment. Mixed effects = effects differed between or within species within the same taxonomic group. Note that studies focusing on more than one taxonomic group are featured multiple times, once per taxonomic group. Those studies have been indicated with matching symbols (i.e. the study * features plants and arthropods).
The early research on community-level effects of noise was conducted by observing the abundance and diversity of bird species as a function of distance from a chronic noise source, such as a busy roadway. This proved an effective method for understanding the effects of noise with clear evidence that species composition, density and abundance were more negatively impacted the higher the noise levels (Reijnen and Foppen, 1995; Reijnen et al., 1995, 1996). Later studies highlighted how species with low frequency calls that overlapped considerably with traffic noise were likely to be impacted to a much greater extent than species with higher frequency calls [(e.g., lower occupancy ()]. However, there were challenges associated with this observational approach such as accounting for confounding variables, including habitat fragmentation, chemical pollution, elevated human activity, and increased mortality (e.g., vehicle strike), that also occur to a greater extent in close proximity to roads (Summers et al., 2011).
The expansion of gas extraction across North America led to the development of natural experiments where areas with noise-generating compressor stations could be compared to areas structurally equivalent to compressor stations but with quiet well pads. These natural experiments largely controlled for the confounding variables associated with other forms of disturbance — such as habitat transformation and human activity — and explicitly investigated the effects of noise on the abundance and diversity of bird species in an otherwise natural environment (). These studies demonstrated that occupancy, diversity and abundance of avian species were negatively impacted by anthropogenic noise (), while also revealing that species exhibited varying levels of sensitivity to noise exposure depending on the extent of vocal masking that they experienced (, ). Larger bodied birds with lower frequency calls were found to use noisy areas considerably less than smaller bodied species with higher frequency vocalizations, which presents a strong selective force shaping avian community structure and species interactions such as predator—prey relationships (, ). However, researchers working in grassland prairies documented an effect of the gas extraction infrastructure, rather than the noise that was associated with it (Nenninger and Koper, 2018), showing the complexity of the mechanisms underlying this disturbance. The physiological costs of noise have also been documented using this natural study system demonstrating impacts to glucocorticoid-signaling and reduced fitness across bird species (), while truly long-term cascading impacts of noise exposure were recently found in a study that revealed chronic noise exposure (15 years) impacted seedling recruitment and woody plant community structure (Phillips et al., 2021). These effects were still in evidence 2–4 years after the removal of noise.
Scientists have also employed playbacks across the landscape to assess experimentally the effects of introduced noise on wildlife communities. The advantages of the playback approach include the ability to control the specific location and duration of noise exposure, as well as the noise source sound level. Furthermore, playbacks allow for the effects of noise to be investigated in isolation of confounding variables that are generally associated with noise disturbance. The first of these landscape-level studies broadcast traffic noise along a 500 m “phantom road” in habitat favored by migratory birds, with the researchers documenting a 25% reduction in bird abundance during playback periods (). Further work revealed that 31% of the bird community avoided the phantom road, while those individuals that remained experienced a reduction in body condition that was associated with an altered trade-off in foraging and vigilance (Ware et al., 2015). There were also age effects with younger birds being impacted by noise to a greater extent than adults (). Subsequent research has demonstrated similar effects of introduced traffic noise on invertebrates, particularly species that rely on acoustic signals in the environment (Senzaki et al., 2020), while breeding birds in North American grassland prairies declined in abundance when exposed to playbacks of noise associated with energy extraction at the landscape scale (; Rosa and Koper, 2022). There appear to be complex interactions between infrastructure, noise and species-specific physiological and behavioral responses that can potentially mediate negative effects, and in some cases noise effects may be dwarfed by the effects of physical structures in natural areas [i.e., oil pumps: (Nenninger and Koper, 2018)]. However, we believe these complexities further highlight gaps in noise research on community ecology where interactions between different ecosystem components, noise, and the health of the community network still exist ().
2. Why do we see differences in community composition due to noise?
Noise can have a profound effect on community composition through a variety of mechanisms (Figure 1 and Supplementary Figure 1). It can directly impact local abundance of different species due to avoidance, increased mortality and decreased recruitment, while indirectly impacting predator—prey and parasite—host interactions, competitor interactions, and species-driven ecosystem structure. Noise can have such a broad impact because species within a community respond differently (e.g., declines, altered predator–prey relationships, etc.). This combination of direct and indirect effects and species variability in response alter composition and structure of the community
FIGURE 1
2.1. Direct effects
One of the direct influences of noise is avoidance behavior; many species will temporarily (Slotte et al., 2004;
While avoidance is a common strategy employed by many species, chronic noise can also alter species abundance through increased mortality. Noise can directly lead to individual mortality through noise-induced permanent injury (excluding hearing loss) or reduction of predator detection. To the best of our knowledge, no examples of noise-induced injury have been demonstrated in terrestrial systems; however, they are unfortunately common in marine and other aquatic systems (
Though not as immediately fatal, animals living in noisy conditions often show altered levels of stress hormones, which are linked to increased stress-responsiveness (
Aside from causing avoidance and increased mortality, noise can alter local populations by impacting reproductive success. This can occur through several mechanisms including decreased breeding rates and decreased juvenile recruitment, as well as altered resource allocation. For example, noise can reduce breeding rates through disrupting detection of potential mates [e.g., greater sage grouse (
2.2. Indirect effects
Changes in one species’ local presence can have indirect consequences across trophic and taxonomic lines, especially if those relocating are predators or parasites. For example, while bird abundance and diversity decreased near chronic playback of traffic noise, grasshoppers and odonates decreased in areas far from the traffic noise, likely because their predators relocated to those places (Senzaki et al., 2020). Changes in the predator assemblage can alter both the communities they move to (increased/different predation pressure) and those they move from (lower/different predation pressure). They may alter the predator–prey relationships with third parties as predators may be forced to switch to uncommonly eaten prey or start eating prey they have never hunted before. Indirect effects of noise can also fundamentally alter the habitat entire species communities live in, for example, if important species like seed dispersers are impacted. By altering the presence of both pollinators and seed predators/dispersers, noise has been shown to alter both the tree and flower communities that are at the foundation of most terrestrial ecosystems (
Noise can also change the interaction with other species in the community. It can alter predator—prey interactions, both through the increase of mortality by predation and through changes in foraging success. Similarly, it can change parasite–host interactions by affecting parasite species’ ability to find their hosts (
Noise has both been shown to reduce responses to predation in some species (Simpson et al., 2015, 2016) but also to increase anti-predator behavior in others (Neo et al., 2014; Shannon et al., 2014, 2016a; Voellmy et al., 2014; van der Knaap et al., 2022). These changes in the effectiveness in which predators hunt their prey can have multiple outcomes. If predators in a noisy area preferentially switch to new or less commonly hunted prey as they become easier prey, this might exacerbate that prey’s local decline, while less drastically affected species may then be temporarily released from predation pressure. Therefore, the outcome of the changes in predator—prey interactions can only be predicted on a case-by-case basis. Furthermore, many of the studies that showed these effects only investigated short-term noise exposure, and might therefore have studied behavioral changes that fade over time.
3. Future directions
There is growing evidence that the impact of chronic noise on animals affects the composition of communities. Direct effects of chronic noise exposure on one species, such as population declines and long-term alterations in behavior, can lead to knock-on consequences for other species in the community. By differentially affecting species, chronic noise has the ability to drastically change community structure and function. Although the growing body of work on this topic is commendable, given the expensive and logistically complex nature of long-term studies, some key knowledge gaps remain. These gaps need to be addressed to ensure effective mitigation of chronic noise exposure. Below, we discuss the main gaps that we see, and suggest possible approaches to fill these.
There is a discrepancy in our understanding of how chronic noise affects different types of communities. The majority of the literature that we reviewed (90%, Table 1) investigated terrestrial ecosystems and diurnal species. While studying freshwater and marine ecosystems is more challenging than studying terrestrial systems, the effects of sound are likely to be different for aquatic communities. Sound propagates further in water than on land, so the same noise source will affect a larger area in the water. Furthermore, terrestrial species can often compensate for acoustic information loss by visual signals and perception. This option is less readily available for aquatic species, as light attenuates rapidly in water. Similarly, nocturnal communities might suffer larger impacts from chronic noise disturbance because of their dependence on acoustic signals.
To understand community impacts of noise properly, we must gain a better understanding of the mechanisms underlying species differences in response to the same noise source (
Besides species differences in response, changing species interactions are likely to be an important influence on community change. Parasites that cannot locate their hosts (
While a lot of the effects of chronic noise on communities have been uncovered with observational studies, understanding the mechanisms behind these effects will require long-term experimental studies. Current experimental studies focus mostly on short-term changes due to noise exposure, while long-term changes in species interactions are likely to have a more profound effect on the community. These long-term changes may be quite different from the changes observed on a short time scale (
Finally, to mitigate effects of chronic noise pollution effectively, we need to know what happens when the noise stops. In contrast to other forms of pollution, noise pollution does not leave long-term traces in the environment once removed. However, does the community immediately change back to pre-noise conditions once noise is removed, or is the changes that occurred due to the noise exposure permanent? The few studies that investigated this have shown mixed results. While white-crowned sparrows (Zonotrichia leucophrys) reverted back to low frequency songs (
Statements
Data availability statement
The original contributions presented in this study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author.
Author contributions
AK, GS, MS, SS, NK, NC, and CW wrote the manuscript. GS, MS, and SS performed the literature research. NC made the figures. AK led the collaboration and guided the writing process. All authors critically reviewed the manuscript, conceived the idea behind the manuscript, approved the submitted version, and revised the manuscript.
Funding
This manuscript was conceived during an interdisciplinary workshop entitled “Allying Conservation & Welfare Research on the Impacts of Human-Generated Sounds on Wild & Captive Animals” funded by the Association for the Study of Animal Behaviour. The funding for the publication of this manuscript was provided by the Canadian Wildlife Service, Environment and Climate Change Canada. During the writing of this manuscript NC was supported by two grants: Japan Society for the Promotion of Science no. PE21015 and Mitacs Accelerate IT29508.
Acknowledgments
We thank the organizers of the workshop for bringing us together and providing a platform for new ideas. We also thank Patrick O’Hara and the Canadian Wildlife Service, Environment and Climate Change Canada for the funds to publish this manuscript.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2023.1130075/full#supplementary-material
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Summary
Keywords
anthropogenic noise, chronic, community, behavior, ecology
Citation
Kok ACM, Berkhout BW, Carlson NV, Evans NP, Khan N, Potvin DA, Radford AN, Sebire M, Shafiei Sabet S, Shannon G and Wascher CAF (2023) How chronic anthropogenic noise can affect wildlife communities. Front. Ecol. Evol. 11:1130075. doi: 10.3389/fevo.2023.1130075
Received
22 December 2022
Accepted
15 March 2023
Published
05 April 2023
Volume
11 - 2023
Edited by
Jarle Tryti Nordeide, Nord University, Norway
Reviewed by
Maria Clara P. Amorim, University of Lisbon, Portugal; Ann Bowles, Hubbs-SeaWorld Research Institute, United States
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Copyright
© 2023 Kok, Berkhout, Carlson, Evans, Khan, Potvin, Radford, Sebire, Shafiei Sabet, Shannon and Wascher.
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*Correspondence: Annebelle C. M. Kok, a.c.m.kok@rug.nl
This article was submitted to Behavioral and Evolutionary Ecology, a section of the journal Frontiers in Ecology and Evolution
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