THE EFFECTS OF ANTHROPOGENIC ACOUSTIC STIMULI (AAS) ON AQUATIC ORGANISMS: A REVIEW

Aria Sharma

ABSTRACT

Anthropogenic acoustic stimuli (AAS), such as the noise produced by the commercial fishing and oil industries, is often present in the environment at much stronger levels than the pollution of natural noise. The scope and magnitude of this type of pollution is thought to affect the physiology of wild animals. Recent work has focused on examining the effects of AAS on the behavioral responses and ecophysiology of animals. Despite the relatively greater amount of research conducted on terrestrial organisms, much less is known about the effects of AAS on aquatic animals. Here, I review the effects of acoustic stimuli on aspects of marine animal reproduction and development, the stress response, and immunological function. However, further research is necessary, in both the laboratory and field settings, to fully understand the lasting impacts of anthropogenic noise on aquatic communities. Indeed, there is a great need for scientists and industry experts to work together to maintain a balance of human productivity and animal livelihood in our world’s waters.

INTRODUCTION

In our drastically changing world, urbanization has posed new concerns for wildlife populations across the world. With urbanization comes many different types of pollution, such as noise pollution (Slabbekoorn and Ripmeester 2008). While there are many natural sources of sound, such as wind, water, and animal behavior, it is clear that anthropogenic noise — defined here as sound originating from humans, such as those caused by pile-driving, commercial shipping, and seismic air guns — are more invasive and occur more frequently than natural acoustic stimuli (Patricelli and Blickley 2006).

The expansion of both the shipping and fishing industries in the modern era has caused a drastic increase in the types of AAS found in the ocean (Anderson et al. 2011b). There has been an average increase of 2.5–3 decibels per decade in the past fifty years, due in part to the doubling of commercial sea traffic. Additionally, the gross tonnage of these vessels has quadrupled in the same time frame (McDonald et al. 2006). Natural noises, such as those of breaking waves, are now added by the sounds generated by commercial shipping, oil exploration, and military and mapping sonars (Hildebrand 2009, Popper and Hastings 2009). Over the past twenty years, oil exploration and construction work have moved into deeper water, which has caused the long-range propagation of seismic signals to increase (Hildebrand 2009).

There has been considerable research conducted on the effects of anthropogenic stimuli on animal populations in the wild (Moller and Swaddle 1997, Erbe 2012, Kight et al. 2012). However, we do not yet fully understand how a wide range of AAS affects an organisms’ physiology. Additionally, there is a deficit in research in the affects of ASS on marine animals. The bulk of current research focuses on terrestrial environments, though aquatic environments arguably suffer as much, if not more, from the detrimental effects of noise pollution (Rabin et al. 2003, Hildebrand 2009, Kight and Swaddle 2011). The pressure waves of sound travel faster in water and attenuate less as distance from the stimuli increases (Kight and Swaddle 2011). Because of how the properties of sound differ underwater as opposed to in open air, the results of terrestrial studies are not as easily extrapolated to aquatic environments.

Thus, I focus this review on the affects of both AAS and other acoustic stimuli on marine animals, and how they may be adapting to it. In light of the reviewed studies, I highlight the need for more cooperation between fishing and oil industry experts, as well as governmental bodies, to develop appropriate standards and policies for usage of AAS in the world’s waters.

BACKGROUND

What is Sound?

Sound levels are referred to in units of decibels (dB), which are relative measures of sound pressure. The decibel scale is logarithmic, meaning that, in air, near silence is measured as 0 dB, while a sound 10 times more powerful is denoted as 10 dB, and a sound 100 times more powerful than near total silence is 20 dB. As a frame of reference, in humans, hearing loss can begin at 85 dB, and exposure to 140 dB causes immediate damage and pain. Underwater dB levels differ from above water due to the pressure differential; above water the pressure corresponds to 20 uPa, while it only corresponds to 1 uPa below water (Finfer et al. 2008). Sound is defined as particle motion and pressure fluctuations. Sensory hair cells in humans’ inner ears and lateral lines are activated in response to particle motion and then convert these motions to electrical signals which then stimulate the nervous system (Slabbekoorn et al. 2010). Thus, any change in either the sound wave or the auditory structures of the humans could cause deep changes in perception, a result that could potentially be true in other organisms as well.

There are a number of acoustic peculiarities that pertain only to an underwater environment. The high density of water allows it to be an excellent medium for sound transmission. Sound travels roughly five times faster in water than in air, correlating to an increase in wavelength. Additionally, sound attenuates less in water, and thus sound travels greater distances at higher amplitude levels in water compared to air. This enables both long-distance communication and the long-distance impact of noise on aquatic animals (Finfer et al. 2008).

In any acoustic signaling environment, differences in abiotic factors, such as humidity, temperature gradients, and topography can generate certain distortions that can interfere with signal effectiveness. Problems in acoustic signaling generally lie in one of two categories: attenuation and degradation. Attenuation is defined as “the process by which all signal components decline equally in intensity due primarily to the dispersion of signal energy over an expanding sphere during transmission.” Attenuation in excess can result from atmospheric absorption, scattering, and boundary interference. Degradation is defined as “the destruction of acoustic signal structure, as a result of reverberation, amplitude fluctuations, and differential attenuation at different frequencies” (Hildebrand 2009). Because attenuation and degradation occur naturally, many species have evolved mechanisms specifically designed to resist these effects and allow for effective signaling in their given habitats (Owings et al. 1986, Rabin et al. 2003, Patricelli and Blickley 2006). Additionally many species alter their daily patterns and locations of callings in order to combat these effects. Modifications to environmental factors alter the transmission of acoustic signals by changing the level of attenuation or degradation in the environment (Rabin et al. 2003).

Types of Noises

Aquatic environments are plagued by both abiotic sources, such as waves, raindrops, and geological events, and biotic sources, such as other animals’ communication and echolocation. In addition to naturally occurring noises, there is increasing awareness that a wide range of AAS form a significant portion of abiotic noise. These sounds do not only affect animal hearing and their ability to communicate, but could also have more immediate and substantial effects on their territoriality (Popper and Hastings 2009). Natural noises in the ocean are thought to range from 20 to 40 dB with increases of 20 dB for certain animal behavior or heavy precipitation (Hildebrand 2009).

Acoustic signals are can be distressed by ambient noise. In order to produce a response from a receiver, signals need to be discernable from background noise. The signal’s detectability is ultimately determined by the relationship of the signal to the ambient noise combined with the receiver’s ability to distinguish between the two (Patricelli and Blickley 2006). Background noise, which results from multiple contributing sources, ensures that receivers can hear vocalizations and that signals are propagated effectively. For marine life, especially for those around commercial fisheries and drilling platforms, ambient noise is largely anthropogenic.

Anthropogenic noises are propagated from a wide variety of sources. Major aquatic contributors to this category include shipping vessels, seismic exploration devices, and construction work (Table 1). Noise from boats is not just generated by large commercial shipping vessels, but also leisure ships and boats that can increase ambient sound levels considerably. The propulsion systems of commercial ships radiate consistent noise. Peak sound levels for individual commercial ships range from 140 to 195 dB, while smaller boats generally range from 150 to 180 dB, roughly a one thousand percent increase in ambient ocean noise (Hildebrand 2009).

Table 1. Typical sources of anthropogenic noise and their dB levels. (Source: Hildebrand 2009)

The second major source of anthropogenic noise is seismic devices, such as high intensity air guns, used around the world for oil exploration and undersea geological studies. In order to glean information about the Earth’s subsurface, these guns fire a high-pressure volume of air into the ocean floor, which in turn generates a sound wave. The pressure of the resultant wave is directly related to the number of air guns, their operating pressures, and the cube root of the total gun volume. These devices can release source-levels of up to 260 dB (Hildebrand 2009).

A third main anthropogenic source of noise, also strongly connected to the fishing and oil industry, is construction work. Aquatic construction work typically involves pile-driving which generates the most noise, is typically found near the shore, and is used for building bridges, wind farms, ports, and other sea structures. Away from the construction impact site, the propagation of noise from pile-driving varies according to the ocean bottom type; at a range of 100 meters, 196 dB have been recorded in the San Francisco Bay (Chan et al. 2013).

There is little known about the full effects on aquatic environments due to an increase in AAS, specially declining fish populations which are so far only attributed to an increase in fisheries, habitat degradation, and runoff pollution by chemicals. However, we know little of the effects brought on by the addition of AAS to aquatic environments. Although humans have utilized water bodies for centuries, these activities have only recently increased in a noisy manner. Sounds can be subdivided into those that are unintentional by-products and sounds that are used for actual measurements (Slabbekoorn et al. 2010). Additionally, sounds can be categorized as high- or low-intensity. Both the intensity of the source as well as the purpose must be taken into consideration in the study of AAS.

High Intensity Noises

There are three commonly agreed upon high intensity noises: (i) pile-driving, (ii) seismic air guns, and (iii) sonar. All three are widely used by the oil industry in the construction of drilling platforms and oil exploration. The first of these high-intensity sources is pile-driving, which is an unintentionally generated sound. There is not enough data to determine how many organisms are killed, whether a specific species is more susceptible to sounds than others, or the “kill zone” distance created by pile-driving. There are no data to support that organisms outside a kill zone even sustain any damage and can be indirectly killed. Another unknown question is whether each individual pile-driving strike is an individual event or whether all the events add together to accumulate damage to marine animals. Currently, our knowledge of the full effects of pile-driving is undeveloped (Popper and Hastings 2009).

A second high-intensity acoustic noise source is that made from seismic air guns. These guns are utilized widely in the oil industry for underwater geological surveys. Another potential use of these air guns is seismic reflection profiling which uses the principles of seismology to outline the properties of the Earth’s subsurface from reflected seismic waves. The use of air guns in the aquatic environment is a more explored area than pile-driving, given the political nature of oil exploration in the ocean. The number of offshore oil platforms worldwide has increased by thousands since the first oil wells were drilled in 1891. Even the exploitation of some renewable sources, such as wind or tidal energy, generate noise through construction efforts (Slabbekoorn et al. 2010). While there is some suggestion in the literature that fish behavior can change with seismic air gun activity, a few have found that several species of fish have negligible responses to air gun emission, other than a transient startle response (Wysocki et al. 2007). This finding underscores that results cannot be generalized from species to species. Therefore, it is necessary to broaden the current spectrum of research to account for a wider variety of organisms.

A final high-intensity source that I will discuss that is widely characterized is sonar. Militaries throughout the world use sonar to detect and find submarines. There is growing concern that high-power sonars could interfere with acoustic communication or the physical-well being of marine mammals and fish (Popper and Hastings 2009). All of these aforementioned noises must be taken together with background noise, which is of lower-intensity but still pervades the entire environment. These background sounds include those produced by shipping and pumping in aquaculture. While intense noises often pass by fish at a quick rate, it is hard for fish to escape general background noise (Slabbekoorn et al. 2010).

Low Intensity Noises

Background noises include low-frequency noises from industrial and recreational activities. Many commercial shipping and aquaculture ventures produce enormous amounts of background, low intensity noises. For instance, over 80% of global freight transport takes place in water through commercial shipping, while commuter transport on noisy ferries occurs on rivers and lakes. The global fishing fleet accounts for 1.2 million vessels in the world’s waters, and ships often have strong motors for towing gear. In addition, recreational vessels are still increasing in popularity, which in turn causes a growing impact on coastal waters, which in turn affect marine organisms (Slabbekoorn et al. 2010).

Outside of the direct biological impact on marine life, AAS may impact food resources around the world. Several countries, including United States, have implemented fishing regulations to curb the effects of human activity on catch rates. Some of these regulations include a reduction in temporal overlap between seismic surveys and fishing activities. Still, regulations often do not take into account that noise can influence stock recruitment over long periods of time, thus reducing catch rates of fishermen (Aguilar de Soto et al. 2013). The response of animals to human-generated sound might range from no overt change in behavior to small movements for the duration of the sound, or potentially larger movements that might displace animals from their normal habitats. This could ultimately cause overall shifts in migration routes, to areas of less food, shelter, or successful reproduction (Mitson and Knudsen 2003, Popper and Hastings 2009, Anderson et al. 2011a, Anderson et al. 2011b).

The Importance of Acoustic Stimuli

Arguably one of the most important behaviors affected by acoustic stimuli is communication, which has lasting impacts on the reproductive success of many aquatic organisms. In the field, communication is defined as the actions of one individual that affect the behavior of another. It is thus important not to take for granted how non-human animals communicate with each other, because we are not yet able to understand the specifics of causality in animal communication. The ability to communicate is an important component of many daily activities in a variety of organisms and relies primarily on organisms’ acoustic vocalizations. Effective use of communication allows individuals to complete daily tasks and is ultimately essential for their survival and reproductive success. Animals use communication to find food, acquire mates, and evade predation (Patricelli and Blickley 2006). In any habitat, acoustic stimuli can be masked by wind, water, and other conspecifics. The increasingly industrialized world, however, forces us to also consider anthropogenic noise as a masker. Masking of acoustic signals increases both with the proximity of the signal and the frequency of additional noise. Thus, as masking increases, communicative signals become increasingly difficult to discern. Historically, species have evolved to minimize acoustic interference between signals and ambient noise. Still, humans have generated new and unique noise patterns that can modify both selection pressures and developmental influences on biocommunication systems.

Despite its importance to the viability of various species, vocal communication amongst fish is an often-overlooked mechanism. Fish commonly produce sounds in spawning aggregations and courtship interactions. These sounds could be essential in the creation of reproductive groups, such synchronizing the release of male and female gametes or facilitating the movements required for mate aquisition (Rollo et al. 2007). The sexual preferences of Atlantic cod (Gadus morhua) can also be influenced by acoustics, as the vocal muscle mass of males was positively related to mating success. These two examples suggest the importance of acoustic communication in fish, though it is not known how the distribution of such communication varies across a wide variety of ocean depths (Slabbekoorn et al. 2010).

Intra-specific communication is not the only role for sounds. Sound enables animals, including different species of fish, to process information about their environment, thereby generating an “auditory scene” and providing them with a 3-D view of the world. This broader view of the world is an added supplement to those animals that have the capability of sight. Generation of an auditory scene may have been a strong factor in the evolution of hearing. Animals would first have needed to learn to detect sounds and only then would they have learned to develop acoustic communication. Thus, the detection of the auditory scene plays a critical role in sound detection. Anything in the environment that disrupts the ability of an organism to detect its auditory scene, such as AAS, could have a detrimental impact on both the life of the individual animal and the survival of the species (Popper and Hastings 2009).

Important Considerations For the Following Studies

It is necessary to recognize that both an organism’s behavioral and biological processes are organized as interdependent levels, each with unique properties (Owings et al. 1986, Smith 1986). For instance, the process of acquiring a mate affects multiple biological processes. In order to accurately analyze one level, it is necessary to take into account the interactions of other levels. Secondly, an organism’s individual auditory capabilities need to be taken into consideration. Bart et al. (2001) found that rainbow trout (Oncorhynchus mykiss) have two significant behavioral changes in reaction to both high and low frequency ambient noise. However, Wysocki et al. (2007) found no significant differences in growth rate and mortality for O. mykiss in relation to chronic noise in the aquaculture. Another important consideration is the lack of data to determine whether the effects of low-frequency tones elicit similar responses as mid-frequency or high frequency tones. The effects of transient sounds, such as pile-driving, can also not be determined (Wysocki et al. 2007). Finally, it is unclear how much overall ambient noise in the marine environment is raised by AAS. It is difficult to compare current levels to pre-industrial days because of the lack of historical data on ambient noise. Additionally, ocean noise levels no doubt vary in different parts of the world, as well as on different shipping routes or harbor ports (Popper and Hastings 2009). Here, I will focus on the relationship between reproduction and development, stress, and immunology in relation to acoustic stimuli and AAS experienced by various marine animals.

REPRODUCTION AND DEVELOPMENT

Reproduction is necessary to propagate genes into the next generation. Studies on reproduction in this arena have examined the lowest sound level that animals can detect at particular frequency (Popper and Hastings 2009). This level is often referred to as the “threshold” of detection or the “absolute threshold” and is measured in quiet environments, such as a soundproof tank. Thus, the threshold may not accurately reflect hearing in the real world. To be detected, a signal of interest must be more intense in locations where there are masking sounds than in locations where no masking sounds are present. Generally, hearing is most difficult, and maskers most potent, when the masker frequencies are closest to those of biologically relevant signals (Popper and Hastings 2009).

In laboratory settings AAS has been shown to be embryonically lethal to fish as well as having a negative impact on overall reproductive success. Banner and Hyatt (1973) found that, in the laboratory setting, a 20 dB increase in ambient sound of fish tanks was lethal to two estuarine fishes (Cyprinodon variegatus and Lepomis macrochirus) during embryonic growth and slowed larval growth. Lagarde (1982) reported similar results on brown shrimp (Crangon crangon) less than ten years later. The authors installed rearing tanks in an oyster farm and compared the growth and mortality causes of shrimp in noise-stressed (30 dB) tanks with shrimp housed in soundproof tanks. Only 50% of noise-stressed females laid eggs, as compared to 80% of the females in soundproof tanks yielding eggs. An interesting finding from this study was inferred from the mean length and growth of the shrimp. Since the mean length of noise-stressed shrimp was 3 mm lower than those in soundproof tanks, another possible line of inquiry was hypothesized that this difference in growth could be accounted for by both metabolic rate changes as well as a behavioral change in the amount of food eaten. At the end of the experiment, the mean weight of shrimp exposed to high background noise was 30 mg lower than their unstressed counterparts. The specific physiological mechanisms underlying the decreased growth and reproductive success of C. crangon have not been elucidated (Lagardere 1982).

In addition to mortality and decreased reproductive success, AAS can adversely affect the morphological development of organisms. A growth study conducted on New Zealand scallops (Pecten novaezelandiae) found that 46% of larvae developed abnormally in all containers that were exposed to pre-recorded playback of a seismic air gun firing at 3s intervals (161–165 dB). The control groups, who were exposed only to the background white noise (132 dB), did not have any larvae develop malformed throughout the duration of the experiment (Fig. 1). Additionally, only 17% of the larvae in the noise tanks developed to the most advanced stage in 24 hours, as opposed to 42% of the control larvae (Fig. 1A). This trend of slowed development continued throughout repeat samplings (Fig. 1B-G). This study strongly indicates the potential negative consequences of high-level sound exposure during larval development. A possible mechanism for the malformation involved morphogenetic changes that are mediated by homeobox genes, which is a yet unexplored research territory (Aguilar de Soto et al. 2013).

Figure 1. Comparative results of the control (C) and noise-stressed (N) groups. The height of the bar indicates (A-G) the percentage of larvae that were in their most advanced stage and the (E-G) percentage of those that were classified as having abnormal development after 66 hours.

(Source: Aguilar de Soto et al. 2013)

Since communication is a vital component of mate selection in aquatic species, fish can be influenced in their choices by ambient noise levels. Female cichlids (Pundamilia nyererei) were exposed to two males in a tank who both made calling sounds. However, one male’s calling sounds were played with background noise and the other without. The males calling without background noise sounds were visited first by 58% of the females, though courtship display was equivalent (Verzijden et al. 2010). The physiological mechanisms underlying this preference are still unknown.

Additionally, allometric correlations with acoustics allow for female mate selection to specifically target male size. This phenomenon has been studied in tree frogs (Hyla microcephala), where male frogs are typically more acoustically attractive when larger. Female tree frogs, when given the opportunity to select mates, landed in noisy male compartments twice as often as they landed in quiet male compartments, or those of lower frequencies. Thus, noisy conditions have been shown to interfere with mate selection, while suboptimal pairing can negatively affect the reproductive success of individuals, and in turn entire populations (Schwartz 1993).

Evaluating the extent of reproductive disruption caused by anthropogenic noises will be enhanced if the possibility of behavioral plasticity is taken into account. While population changes are evaluated at an evolutionary level, plasticity allows for individuals to adjust independently to changes in the environment. Developmentally-plastic adjustments can have evolutionary effects, such as “bridging the gap” until heritable variation becomes available or increases the phenotypic expression of latent genetic variation (Rabin et al. 2003). This field of research has been described in the context of signal use in mammals, generating and responding to vocalizations, which are necessary for the reproductive success of communities. Thus, many mammals exposed to intermittent AAS may not have a large capacity to change the frequency distribution of their calls to avoid the frequency range where AAS interferes. It is unclear how these mammals can compensate for disruptions in vocalizations with other behavioral modifications. Understanding animal communication at a basic level will allow us to ask questions about conservation of species in altered environments. For instance, by expanding our knowledge on the anti-predator communication of California ground squirrels, researchers have been able to extrapolate the impact of highway noise on California ground squirrel communication (Owings et al. 1986). This concept of plasticity is less unexplored in aquatic species.

Given the limited number of marine species investigated, it is unclear whether data from captive rainbow trout can be representative of other species that may differ in hearing ability and in the extent they are dependent on sound. Noise levels could be negatively correlated with the survival of individuals in the wild, though decreases in life span are dependent on a variety of factors, which differ for each life stage. Also of importance would be a better understanding of how such noise affects the development of individuals. Specific birth rates have not yet been determined, which could enhance our understanding of the impacts of noise at the population level.

STRESS

The hypothalamic-pituitary-adrenal (HPA) axis is the part of the endocrine system most traditionally connected to the maintenance of homeostasis through stimulation of the sympathetic nervous system. The axis consists of the hypothalamus, responsible for synthesizing hormones such as dopamine and corticotropin-releasing hormone; the pituitary gland, specifically the anterior pituitary which releases adrenocorticotropin; the adrenal medulla, which secretes catecholamines like epinephrine; and the adrenal cortex, which secretes cortisol, corticosterone, and aldosterone. The increased production of these metabolites are generally interpreted as a stress response (Wingfield 2013).

AAS stimulates the sympathetic nervous system and thus increases glucagon secretion, which, in turn, raises blood glucose levels, and corticosteroids. In rainbow trout (Oncorhynchus mykiss), blood glucose levels were elevated in individuals housed in loud tanks (130 dB) in relation to those housed in quiet tanks (115 dB) (Wysocki et al. 2007). In addition to glucose levels, corticosteroid is a primary stress hormone in many animals. However, research is limited on whether high levels of corticosteroids indicate the presence of any detrimental effects in an organism, or if these high levels of corticosteroids actually indicate a heightened coping ability of the organism. Furthermore, it is necessary to note the induction of a stress response may depend on the type of noise. The noise generated by a ship’s engine, which is variable, results in an increase in cortisol secretion in captive fish. Wysocki et al. (2006) found that in the common carp (Cyprinus carpio), the gudgeon (Gobio gobio), and the European perch (Perca fluviatilis), ship noise (at 153 dB for 30 minutes) stimulated an increase in cortisol secretion. The cortisol secretion increased by 99% in the European perch, 81% in common carp, and 120% in gudgeon as compared to baseline levels (Fig. 2A). Despite the increase when exposed to recorded boat noise, no cortisol level elevation was observed in fish exposed to continuous white noise at 156 dB, a level known to induce temporary hearing loss in the European perch (Fig. 2B). These results indicate that a less predictable stimulus, such as boat noise, is more likely to activate the HPA-axis than a constant stimulus. The ability to adapt to continuous noises must be taken into consideration.

Figure 2. Mean cortisol (+SE) levels of the three investigated species when exposed to (A) ship noise (black) and no-noise (gray) and (B) white noise (black) and no-noise (gray bars). (Source: Wysocki et al. 2006)

Similar results have been found in lined seahorses (Hippocampus erectus) that show high cortisol levels when noise-stressed (Anderson et al. 2011a). The plasma cortisol concentrations for animals in loud tanks (123–137 dB) were 5.8 ng/mL as compared to the animals exposed to quiet tanks (110–119.8 dB) who had circulating levels of 3.9 ng/mL. Though the increases in cortisol levels were small, they indicate a chronic stress response. The effects of the cortisol increase were apparent in other physiologies, such as in immunological function, decreased growth rate, and reduced food intake. This potentially could affect the overall survival and reproductive fitness of organisms, resulting in endangerment or extinction.

The long-term effects of AAS on cortisol levels are still unknown. The cortisol and glucose levels of goldfish (Carassius auratus) that were reared in quiet (110–125 dB) or noisy (160–170 dB) conditions were examined after varying durations of noise. While noise exposure did not significantly affect cortisol or glucose over a long period of 60 min, there was a significant increase in short-term cortisol levels. Mean cortisol levels tripled after 10 min of noise exposure before returning to baseline by 60 min (Fig. 3) (Smith et al. 2004).

Figure 3. Mean (+SE) of goldfish plasma cortisol levels. The asterisk denotes a level significantly different from the control (P=0.01) (Source: Smith et al. 2004)

Additionally, some captive fish exhibit cardiac stress, noted by heart rate elevation and increased muscle metabolism, in response to AAS (Graham and Cooke 2008). Largemouth bass (Micropterus salmoides) were exposed to the sound of a combustion engine, an electric motor, and a canoe paddle. Their cardiac output (CO), heart rate (HR), and stroke volume (SV) were measured and compared to a baseline (baseline CO: 29.22 mL/min-kg, resting HR: 39.63 bpm, baseline SV: 0.75 mL/kg). The combustion motor elicited the greatest cardiac disturbance (CO: +43.67%, HR: +67.08%, SV: -23.71%) (Fig. 4). This study indicates that the stress fish exhibit in response to boating disturbances extends even to the cardiac function of the organisms. This study also monitored fish stress in real time, as the bass were not subjected to a playback or simulated boat noise, indicating that the results could be extrapolated to real world scenarios.

Figure 4. Maximum values achieved in each treatment for the largemouth bass following treatment (x: canoe paddle, y: electric motor, z: combustion engine). (Source: Graham and Cooke 2008)

Neurologically, it is unclear whether the psychological mindset of stress as a result of anthropogenic noise can be perceived in animals. One study found that captive belugas (Delphinapterus leucas) that were subjected to playbacks from a drilling platform had no detectable increase in blood epinephrine or catecholamines. However, this result could not be necessarily extrapolated into the wild (Thomas et al. 1990). Romano et al. (2004) more recently examined noradrenaline, epinephrine, and dopamine levels in a wild-bred beluga. Mean norepinephrine, epinephrine, and dopamine levels increased significantly after exposure to the sound of a firing seismic air gun, or roughly 198–226 dB (by 337.75 pg/mL, 30.92 pg/mL, and 37.42 pg/mL respectively) (Fig. 5). These same three levels displayed a positive correlation to sound levels.

Figure 5. Means (± SE) of (a) norepinephrine, (b) epinephrine, and (c) dopamine for three experimental groups (control, E1: low sound exposure, E2: high sound exposure). Low sound exposure had a frequency of 0.4 kHz, while the high sound exposure had a frequency of 30 kHz. (Source: Romano et al. 2004)

The same study measured aldosterone response in a bottlenose dolphin (Tursiops truncates) after the firing of a water gun (213–226 dB) and found that aldosterone increased by 50.48 pg/mL in response to the noise (Fig. 6) (Romano et al. 2004).

Figure 6. Group differences in serum aldosterone after being exposed to the sound of a water gun firing. (Source: Romano et al. 2004)

It is unclear whether AAS, in addition to causing hormonal disruptions, can cause long-term physical damage to the HPA axis that might have lasting impact on the maintenance of homeostasis in aquatic organisms. Research is limited on the long-term impacts of noise stressors on the HPA axis for animals, though information exists on the other stress response-inducing factors in birds. For instance, corticosterone levels are negatively associated with immune responses, survival, and song syllable diversity in three species of birds (barn swallows (Hirundo rustica), song sparrows (Melospiza melodia) and white storks (Ciconia ciconia)) (Kight and Swaddle 2011). Future studies are necessary to investigate the possibility that sporadic and continuous acoustic responses may be detrimental to wildlife communities in the long run. Still, there is the possibility that certain stress responses are plastic, and that control over AAS produced by major industries could allow animals to recover from any perceived damage.

IMMUNE FUNCTION

Noise related effects of stress on the HPA axis could eventually lead to negative effects on the immune system, even across generations. One measure of the immunologic function of animals is the heterophil-to-lymphocyte ratio (H:L), which allows for the indirect measurement of lymphocyte levels in various species. Heterophils are granular leukocytes and contain antibodies. Because cortisol induces the destruction of lymphocytes and increase in blood heterophils but slows the wound healing, scientists involve the H:L ratio as both an immunological and stress measure in animals (Anderson et al. 2011a).

The majority of research of AAS on the immune system has been conducted in laboratory settings on non-marine mammals. Maternal stress in mice (Mus musculus) was examined by repeatedly exposing pregnant mice to an 85dB alarm bell before testing the pups’ immunologic function using titers to Herpes Simplex I and Tuberculosis. The lymph-proliferative activity and immunoglobulin G was higher in noise-stressed mice. Additionally, the pups from exposed mothers had an average thymus weight of 24.92 mg, as compared to 26.63 mg of non-prenatally stressed pups (Sobrian et al. 1997). Another study found that, when exposed to ten 15 minute periods of loud noise (measured at 85dB) per day for three weeks, rats (Rattus norvegicus) display decreased immune responses — as found by increased immunoglobulin levels, decreased T cell counts, and decreased phagocytic activity. The length of exposure to the loud noise influenced the observed physiological changes. For instance, natural killer cells exhibited higher levels of activity after 7 days of exposure, as compared to those of the control group. In this study, different components of the immune system did not necessarily predict each other. Thus, it is possible that chronic noise exposure differentially impacted the immunity of the rats (VanRaaij et al. 1996). However, the results of these studies can be used to generate hypotheses to be explored and tested in marine animals.

Concerning marine life, cell counts have been reported to also be affected in response to AAS. Noise stressed (123–127 dB) seahorses (Hippocampus erectus) demonstrated significant and variable heterophils and significantly higher and more variable H:L ratios (Anderson et al. 2011a). Heterophils were a greater proportion of the leukocyte population in loud tanks than in quiet tanks (35.8% vs. 22.5%). Consequently, the H:L ratio of seahorses in loud tanks was significantly higher than seahorses in quiet tanks (0.88 vs. 0.36). These results indicated a significant secondary stress undertaken by seahorses in loud tanks. In another aquatic experiment, for a bottlenose dolphin (Tursiops truncates), the absolute monocyte count of the noise-stressed individual — who was exposed to the firing of a water gun — was, on average 192 cells/mL less than unstressed organisms (Fig. 7) (Romano et al. 2004).

Figure 7. Group differences in absolute monocyte counts for a bottlenose dolphin after exposure to the sound of a water gun firing (213–226 dB). (Source: Romano et al. 2004)

IMPLICATIONS AND DISCUSSION

Here I have shown that AAS can have deleterious effects on organisms. This can occur via the masking of vocalizations and thus communication, as well via chronic activation of the HPA axis leading to decreased growth and reproduction. AAS has also been shown to cause failures in mate attraction (Schwartz 1993, Patricelli and Blickley 2006, Verzijden et al. 2010). This failure could contribute to reduce the total population density of species, and it underlines the need to investigate potential long-term effects of AAS on marine populations (Aguilar de Soto et al. 2013).

The studies I have received have shown that potential effects from intense AAS sources, such as those generated by the oil and shipping industries, can produce stress responses in whales, fish, and seahorses (Romano et al. 2004, Smith et al. 2004, Wysocki et al. 2006, Graham and Cooke 2008). Negative effects could also include physical tissue damage or hearing loss that could, in turn, decrease the fitness and survival of the organism (Slabbekoorn 2012, Smith 2012, Bruintjes and Radford 2013). Behavioral changes might also take place, resulting in animals leaving their normal feeding or breeding grounds (Smith 2012, Bruintjes and Radford 2013, Read et al. 2014, Rendell et al. 2014). More field research is necessary to evaluate the extent to which various AAS sources affect organisms in the wild.

Chronic AAS, such as those produced by commercial shipping and recreational boating, can be less intense because of their lower dB levels but cause an overall increase in background noise in various locations (Hildebrand 2009). While fatality to organisms may not be a primary concern in these areas because the sounds are less intense, these sounds can still result in the masking of natural sounds in reproductive behaviors or could cause adverse consequences on the immune system (Popper and Hastings 2009).

It is important for conservationists to determine the most effective methods of reducing anthropogenic noise to develop informed conservation management strategies, ultimately maintaining population viability. One potential method to reduce AAS in the aquatic environment is the construction of artificial sound barriers in harbors or ports (Slabbekoorn and Ripmeester 2008). Other possible solutions are the institution of a noise tax on fish farms, reduction of fishing or passenger transport methods, and port closures during acoustically important times, such as breeding season (Bayne et al. 2008).

It might be possible to investigate the impact of AAS on fish diversity and density by partnering with commercial fishing and oil industries. Several offshore platforms exist that generate high underwater noise levels from compressors and human activity, while others are more silent. Freshwater systems, which are often more accessible, can be explored experimentally through the use of artificial noise sources in comparison to quiet, control locations (Slabbekoorn et al. 2010).

Historically, the oil industry has operated in shallow water (depth < 500 m). This has taken a turn in the 21st century as geological exploration is conducted in increasingly deeper waters. Because sound propagates at a greater distance in deep water, seismic exploration is a significant contributor to increased ambient noise in the Gulf of Mexico, both the North and South Atlantic, and in the North Sea. The world’s water-systems are interconnected in a way that one event will not produce one single event, but will instead have a ripple effect (Hildebrand 2009).

LIMITATIONS

The majority of this research has been conducted in a controlled artificial lab setting, due to the presence of confounding factors when examining wild environments, as well as the lack of effective detection methods. However, wild environments contain many more factors that influence animal physiology. Future studies on the impact of AAS on the nature of reproductive behavior must be explored in the habitats of free-living animals, to take into account both natural behavioral and physiological responses.

Another issue with analyzing a laboratory population is that, to my knowledge, no study has been conducted on the effect of AAS on animals throughout their entire lives. Instead, studies have focused on development over periods of time less than three months. This coincides with a need to study the effects of chronic AAS over the course of various life-history stages, as opposed to just intense and periodic outbursts of environmental noise.

In addition to the need to measure a wider variety of taxa as well as a wider threshold of dB levels, there is somewhat limited research available on some types of sounds. For instance, some aquatic species, such as fish in the Alosinae family, can detect ultrasound noise, which could have detrimental impacts at the levels produced by AAS. Auditory mechanisms that require more research include determining the factors that actually elicit responses, such as the duration, amplitude, frequency, and predictability of noises.

One must also take into account that different sources have different acoustic characteristics. Furthermore, the measurable effects result from the sound actually perceived by the animal. Describing a sound in terms of its peak or pressure only shows one part of the larger characterization of the AAS, especially when the sound is relatively long lasting or has a complex temporal structure. It is important for future studies to keep in mind the importance of standardizing the characterization of sound sources. One significant step in this direction has been the development of Sound Pressure Levels (SPL) as a widely used metric in the field, thus allowing for cross-study comparisons (Popper and Hastings 2009).

It is also possible that some animals may habituate to AAS over time. For example, Magellanic penguins (Spheniscus magellanicus) only exhibit stress to tourisms at highly trafficked periods, not at moderately trafficked periods (Fowler 1999). Similarly, the stress response of Galapagos marine iguanas (Amblyrhynchus cristatus) to tourism has shown some adaptation over time (Romero and Wikelski 2002). Both these organisms exhibit lower corticosterone levels in the areas that are more frequently visited by tourists. It is unclear whether other aquatic organisms are also able to acclimate to long-term stressors over time. Additionally, certain fish or sea mammals can alter their migration patterns in response to common shipping routes (van Opzeeland and Slabbekoorn 2012, Rendell et al. 2014, Rice et al. 2014) .

There is the further issue of whether the data collection methods used by researchers can possibly impact animal behavior. For example, studying aquatic organisms’ behavior from a research ship may produce results that would not occur if the ship was not present (Mitson and Knudsen 2003). These protocols will need to be elucidated further in the future.

There are two main caveats to this specific review. One is that most of the literature reviewed describes the response of aquatic animals to noises ranging from 65 to 130 dB, though majority of animals encounter amplitudes that are at the lower end of the scale. While the majority of ambient terrestrial natural noises are between the range of 27–80 dB, anthropogenic noises tend to focus on the range of 50–116dB (Table 2) (Rabin et al. 2003). This is discrepancy can be extrapolated to aquatic environments as well. Thus, results may not be directly comparable to field environments. Additional work is necessary to determine what patterns and mechanisms observed here are actually applicable to wildlife. Future research should expand our understanding to a more diverse array of taxa, such as reptiles, amphibians, and invertebrates, all of which are underrepresented. As the diversity of research on species and populations increases, comparative studies may allow us to determine the mechanisms that cause different reactions in different species.

Table 2. Representative Sound Pressure Levels (SPL) under either “natural” or anthropogenic conditions. (Adapted from Rabin et. al 2003)

SUMMARY

I have reviewed how AAS can adversely affect the reproductive, developmental, stress response and immunological capabilities of a variety of marine animals. Sound is of critical importance to aquatic animals in many aspects of their lives, such as the previously mentioned auditory scene or mate acquisition. Commercial shipping or oil drilling, among other sources of AAS, interferes with the detection of sound and thus can potentially impact the lives of marine organisms. These sounds have the potential to not only affect individuals, but also the survival of their entire species. The results of my investigations suggest that while AAS can be harmful, they can also play an integral role in animal development.

The effects of physiological responses may not be reversible if noise is present during key developmental stages. Still, there is a possibility that responses may have the ability to recover from short-term damage, thus resulting in fewer long-term consequences for both individuals and populations. Researchers studying the adverse effects of AAS should link both genetic and cellular responses to physiological and behavioral responses to account for long-term changes that would possibly only be seen evolutionary or hereditarily.

Though field studies are incredibly important, laboratory research has some unparalleled benefits, including the ability to easily isolate responses to acoustic stimuli, as opposed to confounding factors, such as light pollution, habitat structure, and unrelated human activity. Additionally, laboratory settings can help to interpret the responses of animals that might not be easy to study in the field. If specific physiological mechanisms are implicated in multiple cross-species tests, it is possible that multiple mechanisms are conserved across vertebrate species and that results can be extrapolated from species to species.

Conservation efforts benefit from research that investigates naturally occurring processes. Urbanization, and its effects on the subsequent increase in AAS, has been implicated in the negative detrimental physiological responses of both terrestrial and aquatic species (Anderson et al. 2011b, Kight and Swaddle 2011). The studies I have reviewed have mostly shown that while AAS affects aquatic organisms, it is less understood to what extent the effects continue over long periods of time. Further investigation into the effects of AAS on aquatic organisms will allow the advancement of the conservation efforts needed to protect animals from the dangers of urbanization.

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