A number of studies have demonstrated effects of noise from large ships on a variety of cetacean species, including Cuvier’s beaked whale, North Atlantic right whale, beluga and fin whales. These studies provide a hint that ship noise can reduce a whale’s foraging efficiency; elevate the risk of ship strike; and cause physiological stress that is detectable in hormone levels. Whales have evolved in an ocean environment that becomes naturally noisy during storms and surf zones, and they have evolved some mechanisms to compensate for noise. Fin whales change their song characteristics to try to maintain communication in high levels of shipping noise. There is some evidence to suggest that killer whales can compensate for increases in ambient noise by lengthening their calls or increasing the source level of social calls. There is no evidence that killer whales can adjust their echolocation patterns to compensate for masked signals used in forag. Northern and southern resident killer whales have been listed under the relevant endangered species legislation of Canada and the US. Both countries have recognized prey depletion, contaminants and anthropogenic noise as risk factors in the whales’ current conservation status and threats to be addressed to promote recovery; National Marine Fisheries, and no information on the upper limit to the whales’ compensatory mechanisms. Similar data on southern resident killer whales (collected by JS) were examined for comparative analyses, but only two natural experiments were observed. Data were collected using an electronic theodolite (Pentax ETH-10D with a precision of ±10″ of arc) connected to a laptop computer equipped with custom software. Positions of surfacing animals (horizontal and vertical angle coordinates) were located using the theodolite and directly recorded into the laptop computer using THEOPROG. At each surfacing, the team recorded the focal whale’s alpha-numeric ID, each time the whale surfaced to take a breath, and any corresponding surface active behavioral events such as breaches, pectoral fin slaps and tail (fluke) slaps. Accuracy of each whale position was confirmed by the laptop operator by viewing the positions as they were plotted in real-time. Any deviation or noticeable gap in surfacing was reviewed and confirmed by the theodolite operator. We defined a moderate change as a 20–50% change in a variable, based on the 25% change in swimming speeds of female killer whales to a single boat parallelling the whale at 100 m. We defined an extensive change as a >50% change in a variable, based on the 90% change in path smoothness when a boat leapfrogged the whale’s path at 150–200 m. Importantly, the severity score is meant to differentiate between minor/brief responses (0–4), those that could affect foraging, reproduction or survival (4–6), and those (7–9) that could affect vital rates.We assessed 42 theodolite tracks containing ship transits to find natural experiments that could be used to model the probability of a whale responding. Of the 42 tracks considered, 35 could be considered in a before-during natural experimental framework, with sufficient information to quantify changes in whale behavior before and during a ship transit. The 7 tracks that had to be dropped contained insufficient information about whale behavior before and/or during the ship’s transit to evaluate response; sparse information on the ship’s track was not the limiting factor. Scoring each experiment as either a response or a non-response required using all values greater than or equal to some severity score cutoff as a somewhat arbitrary threshold.
Northern resident killer whales showed moderate (severity score 2–4) responses to the presence of the large ships that use Johnstone Strait in summer months, but behavioral responses were best explained by combinations of time (Year and Month), age of the animal, number of ships (CAR, COL and TUG) and the broadband noise level received by the whale (RL_rms). Evaluating the effects of ship traffic on killer whale behavior is overwhelmingly influenced by a somewhat subjective and seemingly arbitrary decision about the severity score that one uses to indicate a response. The response variable we measured represents current best practice in quantifying exposure and response of marine mammals to noise, but future studies may need to consider more ecologically relevant response variables. We did not measure vocal behavior of killer whales (echolocation or call rates, source levels etc.), and ultimately, one would want to test whether foraging efficiency or prey intake were affected by these noise levels. The metabolic cost of swimming in killer whales is fairly flat across the range of speeds observed in this study, so in general, these behavioral responses are expected to carry minor energetic costs in terms of increased energy expenditure, with two important caveats. First, the cost to females of having a calf swim in echelon formation is already high, at a time when lactating females may already be energetically stressed, so if female killer whales truly are more responsive than males to large ships (Model 3), then increasing their travel costs would be a conservation concern (Williams et al., 2011). Secondly, this study only looked at overt behavioral responses from surface observations. If ship noise is reducing prey acquisition through acoustic masking of echolocation signals, causing whales to abandon foraging opportunities, or by repelling fish, this study would have no way of detecting those effects. The energetic cost of ship noise may be substantial in terms of reduced prey acquisition (through masking or disruption of feeding activities), even if the energetic cost of avoiding ships is relatively low. Similarly, we have not considered any physiological (i.e., hormonal) stress responses to ship noise, which have been shown to be important in other cetaceans.
Ship noise and cortisol secretion in European freshwater fishes
Underwater noise pollution is a growing problem in aquatic environments and as such may be a major source of stress for fish. Anthropogenic noise can alter the behavior of whales, birds and fish and thus have long term direct or indirect consequences on the behavior, fitness and ecology of a species. Certain whale species react to approaching vessels by changing their vocalizing, resting and migration behavior. Recreational activities, like boat fishing, have been found to be a major disturbance in several species of migrating water birds resulting in increased alertness, escape activities and energy expenditure. The effects of boat noise on fishes have mainly been investigated in the marine environment within the framework of population assessment and better management of catch rates for the fishing industry. Avoidance reactions to vessel noise of marine species such as herring (Clupea harengus) and cod (Gadus morhua) and the freshwater fishes rudd (Scardinius erythrophthalmus) and roach (Rutilus rutilus) have been studied in the field. It was shown that fishes actively avoid specific kinds of vessels with vertical and horizontal displacements. There is some indication that noise can elicit an endocrinological stress response in fish as well. Sverdrup et al.
(1994), Santulli et al. (1999) and Smith et al. (2004) reported changes in cortisol and other biochemical parameters in Atlantic salmon (Salmo salar) and European sea bass (Dicentrarchus labrax) after air-gun detonation or underwater explosions and in goldfish (Carassius auratus) after exposure to 160 dB white noise. The aim of the present study was to investigate whether and to what degree ship noise encountered in rivers and lakes could produce a similar cortisol increase in three selected species of common European freshwater fishes. Cortisol is considered as the principal corticosteroid secreted by the teleost fish adrenal system in response to acute and chronic stress. Its concentrations in the blood, plasma, tissue, and recently also in the holding water has been commonly used to monitor stress responses. We exposed fish to ship noise recorded in the field and to continuous Gaussian noise with a relatively equal energy distribution over a broad frequency spectrum. Both noise type were then applied at physiologically relevant levels known to result in temporary hearing loss in fish species with specialized hearing. In the present experiment, we chose species with quite different hearing abilities to test whether hearing specialist species like common carp (Cyprinus carpio), and gudgeon (Gobio gobio) with excellent hearing abilities were more affected by noise than a hearing generalist, the European perch (Perca fluviatilis). Similarly, we hypothesized that a dynamic and thus unpredictable noise source with varying levels and frequency content like that associated with the passage of various vessels in the field would elicit a different and perhaps more intensive stress response than more consistent noise to which an organism could possibly become habituate
Experimental setup
Each individual was subjected to three different test conditions: Boat noise, Gaussian noise, and no-noise control. In each test condition, a single fish was placed in a plastic bucket (21 cm height, 22 cm diameter, 12 cm water depth) containing 3 L of water for 30 min. The water in the bucket originated from a 200-l storage water tank, that did not contain any fish. Cortisol levels were measured in 1 l samples of the storage tank water to control for the potential presence of waterborne substances that could bind to the cortisol antisera used. The levels of immuno -reactive cortisol in these samples were below the detection limit of the assay. The mean temperature during experiments was 22 ± 1 C. After the noise exposure period, the fish were removed from the bucket and 1 l of water was taken and subjected to the cortisol extraction procedure described below. Animals were not fed for at least 20 h prior to experiments.
Result: These levels were always above 0.1 ng/l water/g fish. The levels of cortisol in storage water were below the level of detectability in our assay, hence they were less than 2.6 pg/l water. Hence the presence of fish was associated with at least a 280-fold increase in cortisol concentration for a 7-g fish. In the experiment cortisol levels following a 30-min exposure to boat noise were significantly higher in all three species. The mean increase in cortisol was about 99% over control values in European perch, 81% in common carp, and 120% in gudgeon. Exposure to Gaussian noise did not produce a significant change in cortisol levels relative to the controls. The no-noise control levels were similar in both control measurements for common carp (average of 0.22 ± 0.05 ng/L water/g fish for boat noise controls versus 0.16 ± 0.01 ng/l/g for Gaussian noise controls) and the European perch (0.15 ± 0.01 ng/l water/g fish boat noise, 0.25 ± 0.07 ng/l water/g fish Gaussian noise). The control levels in gudgeon differed being 0.34 ± 0.09 ng/l water/g fish for boat noise but 0.1 ± 0.04 ng/l water/g fish for Gaussian noise controls.
It is often empirically difficult to causally link human activities to specific changes in animal behavior. To date, the impacts of navigation have mainly been linked to hydraulic forces challenging swimming performance in juvenile freshwater fish, or indirect effects imposed by the development of suitable waterways such as migration barriers, pollution habitat loss, and biotope simplification. The factor noise and its impact on fish behavior and physiology has been neglected with only a few exceptions. Active avoidance of vessels in dependence of the amount of noise emitted have been found in cod, herring, and also in the freshwater species rudd and roach. These individual observations only allow to speculate on the impacts of noise on the population. Our results show that ship noise can elicit a cortisol stress response in different species regardless of their hearing sensitivities. This is relevant because underwater noise pollution is a growing environmental problem and some evidence exists that noise disrupts developmental processes and growth in aquatic organisms including fish. Cortisol has detrimental effects on growth, sexual maturation and reproduction, immunological function and survival in fish. Stress challenges an organism’s homeostasis acting thus as a threat to its healt and the level of stress can serve as an important welfare indicator.
Based on our data and on the fact that intermittent ship noise usually goes on for a longer time than the period used in our experiments, more future long-term studies should be directed towards a multifactorial analysis of ship trafficking effects on fish. It is necessary to expand these studies to include analyses of fish behavioral responses to different types of vessels in the field. In addition, hydrology, season, community composition, and habitat structure should be considered as compounding factors that could affect fish populations. These studies could then be used to develop plans for effective protection. Onboard noise levels have become a significant element in the construction and design of ships in recent years with regard to passenger comfort and navigation safety. We would suggest that similar effort should be taken to lessen the underwater noise emission.
Effects of ambient and boat noise on hearing and communication in three fish species living in a marine protected area (Miramare, Italy)
Noise can be defined as an ‘‘unwanted sound” that affects animals by causing stress, increasing the risk of mortality by unbalancing predator/prey detection, and by interfering with orientation and sound communication, especially in the reproductive context. The amount of marine noise pollution generated by humans has been increasing significantly within the last decades not only in highly populated coastal areas, but also in the open ocean This raises a broad concern on the extent of negative impacts on marine life. Human-made noise in the sea can be categorized as high-intensity and acute such as the noise produced by military sonar, pile driving and seismic explorations, or lower-level and chronic such as ship noise. Investigating the impact of boat noise on fish species is particularly relevant for sensitive areas located in highly populated coastal zones, such as the WWF-Miramare Natural Marine Reserve. The latter is an UNESCO-MAB Biosphere reserve located in the Gulf of Trieste (North Adriatic Sea, Italy). Compared to more remote Mediterranean Marine Protected Areas (MPAs), the level of human presence around Miramare MPA is extremely high. The site is close to a touristic port characterized by high recreational boat traffic. It is also less than 8 km away from the city of Trieste, an important seaport with more than 48 million tons of ship traffic per year. Nonetheless, the reserve’s coastline (1700 m) and offshore area (120 ha) are densely populated by different fish species, most of which spawn during summer. The aims of the present study were to investigate whether three representative vocalizing fish species in Miramare, i.e. S. umbra, C. chromis and G. cruentatus, are adapted to the ambient noise and determine the degree to which the noise of a cabin-cruiser– the typical boat type used both inside and around the reserve – affects both their hearing sensitivity and their ability to detect conspecific sounds and thus their intraspecific acoustic communication.
S. umbra (Linnaeus 1758) is one of the five species of the family Sciaenidae (drums, croakers) living in shallow coastal waters of the Mediterranean Sea. During the reproductive period, S. umbra generates a chorus consisting of overlapping, short-lasting broadband pulses with main energies below 1 kHz. Preliminary observations showed that boat noise can mask the chorus, especially between 200 and 300 Hz. C. chromis (Linnaeus 1758) is the only representative of the family Pomacentridae (damselfishes) in the Mediterranean Sea . It lives in shoals at depths ranging from 3 to 30 m. During the spawning season (June–September), males prepare a benthic nest and court females using visual displays, known as signal jumps (Abel, 1961). These are accompanied by acoustic signals, i.e. broadband single pulses called ‘‘pops”, peaking at about 400 Hz. G. cruentatus (Gmelin 1789) is a small benthic member of the family Gobiidae (gobies) common in the Mediterranean Sea and in the Western Atlantic Ocean. Throughout the year, it uses crevices in the rocks as shelters , defending them vigorously from intruders with both visual and acoustic displays. The acoustic repertoire of G. cruentatus consists of four low-frequency sound types, emitted during territorial encounters.
Sounds of S. umbra were recorded at night (between 21:00 and 23:00) on 26 April and 23 July 2007 from a boat in water depths of 4–12 m at four different locations. The experiments were conducted within a range of 30 m to artificial rocky reefs located in the core zone of the reserve in which fish are abundant, but at unknown distances to the individual fish. The recording conditions were: sea state 1 (Douglas scale), wind speed 10–15 km/h, 15% clouds in April, and sea state 1, wind speed 7–10 km/h, 0% clouds in July. Sounds of C. chromis were recorded on 25 July during day time at three different locations within one nesting area in a water depth of 4 m. Additional recordings were done at distances of 30–50 cm from nesting males displaying courtship behaviour (signal jumps). The recording conditions were: sea state 0, wind speed 1–2 km/h, 0% clouds. Sounds were recorded either on a Marantz PMD 660 digital recorder (in April) or on a DAT recorder Sony TCD 100 (in July) using a hydrophone Brüel & Kjaer 8101 powered by a power supply Brüel & Kjaer 2804. Absolute sound pressure levels (LLFP, L-weighted, 5 Hz–20 kHz, RMS fast) of the sounds were simultaneously measured with a sound level meter connected to the second output of the power supply. S. umbra showed lowest hearing thresholds at 300 Hz, whereas both G. cruentatus and C. chromis had a maximum auditory sensitivity at 200 Hz. The drum showed a broader hearing bandwidth and lower thresholds than the damselfish and the goby, detecting tone bursts up to 3000 Hz. On the other hand, no consistent AEPs could be obtained for frequencies higher than 600 Hz in
C. chromis and higher than 700 Hz in G. cruentatus at the highest possible test level (136 dB re 1 lPa). Baseline hearing thresholds recorded under quiet lab conditions were barely masked by ambient noise in all three species. In contrast, auditory thresholds increased considerably during boat noise exposure at all frequencies by up to 35 dB in S. umbra, 20 dB in C. chromis, and 10 dB in G. cruentatus as compared to the sensitivity under ambient noise conditions. The largest threshold shifts between ambient and boat noise conditions occurred in the frequency range in which all three species were most sensitive to sound. This threshold shift decreased with increasing frequency (35 dB at lower frequencies vs. 10 dB at 1 kHz) in S. umbra. Similarly, in G. cruentatus, the smallest difference between the BN and the AN thresholds was at the highest frequency tested (700 Hz).
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