Integrating Techniques: A Review of the Effects of Anthropogenic Noise on Freshwater Fish

In recent years, the effects of anthropogenic noise on freshwater fish has been of increasing interest for fishery managers due to rising levels of this background noise. While it is clear that anthropogenic noise can have important impacts on mammals and marine fish, much less is known about these effects in fresh water. The influence of anthropogenic noise on freshwater fish can be quantified using the same methods as with marine species — through measuring changes in behavioural and physiological outputs. Here, we briefly review the literature regarding behavioural and physiological impacts of noise pollution on freshwater fish and further note the lack of incorporation of both behavioural and physiological measures within current studies. We call for an increased research emphasis on possible effects of anthropogenic noise on freshwater fish and further suggest that the integration of behavioural and physiological techniques is critical for a full understanding of these effects. While freshwater fish face many stressors, it is unclear how important anthropogenic noise really is and this issue can only be properly resolved through careful study

Ontogeny of visual and mechanosensory structure and function in atlantic menhaden Brevoortia tyrannus

The importance of visual, mechanoreceptive and auditory inputs to escape responses was examined in larvae of the Atlantic menhaden (Brevoortia tyrannus) presented with a simulated predatory stimulus. Ontogenetic changes in the retina, superficial neuromasts and auditory bullae were examined in concert with behavioral trials in which sensory inputs were selectively blocked. Menhaden larvae showed a decrease in cone photoreceptor density and first developed rod photoreceptors when their total length (TL) reached 8-10 mm; they began summing photoreceptive inputs at 12-14 mm TL. Inflation of the auditory bullae was complete by 15 mm TL. The proliferation of superficial neuromasts varied depending on their location, with cephalic superficial neuromasts decreasing in number beginning at 19 mm TL and numbers of trunk neuromasts continuing to increase throughout the larval period. In behavioral trials, responsiveness and the reactive distance to the approaching probe increased with increasing larva total length when all sensory inputs were available (control larvae). When visual inputs were blocked, responsiveness was lower than in control larvae, but still increased ontogenetically, while reactive distance showed no difference between control larvae and those lacking visual information. When neuromasts were ablated, ontogenetic increases in responsiveness and reactive distance were absent. Inflation of the auditory bullae had no discernible effect on behavior. The anatomical and behavioral results suggest that both vision and mechanoreception are used to trigger a response to a looming predatory stimulus and that mechanoreception, but not vision, contributes to the timing of the response. Ontogenetic improvements in performance are attributed mainly to neuromast proliferation and not to ontogenetic changes in the retina

The effects of stimulus parameters on auditory evoked potentials of Carassius auratus

Whole-brain responses to sound are easily measured through auditory evoked potentials (AEP), but it is unclear how differences in experimental parameters affect these responses. The effect of varying parameters is especially unclear in fish studies, the majority of which use simple sound types and then extrapolate to natural conditions. The current study investigated AEPs in goldfish (Carassius auratus) using sounds of different durations (5, 10, and 20 ms) and frequencies (200, 500, 600 and 700 Hz) to test stimulus effects on latency and thresholds. We quantified differences in latency and threshold in comparison to a 10-ms test tone, a duration often used in AEP fish studies. Both response latency and threshold were significantly affected by stimulus duration, with latency patterning suggesting that AEP fires coincident with a decrease in stimulus strength. Response latency was also significantly affected by presentation frequency. These results show that stimulus type has important effects on AEP measures of hearing and call for clearer standards across different measures of AEP. Duration effects also suggest that AEP measures represent summed responses of duration-detecting neural circuit, but more effort is needed to understand the neural drivers of this commonly used technique

The contribution of the lateral line to \u27hearing\u27 in fish

In the underwater environment, sound propagates both as a pressure wave and as particle displacement, with particle displacement dominating close to the source (the nearfield). At the receptor level, both the fish ear and the neuromast hair cells act as displacement detectors and both are potentially stimulated by the particle motion component of sound sources, especially in the nearfield. A now common way to test ?hearing\u27 in fish involves auditory evoked potentials (AEPs), with recordings made from electrodes implanted near the auditory brainstem. These AEP recordings are typically conducted in enclosed acoustic environments with the fish well within the nearfield, especially for lower frequencies. We tested the contribution of neuromast hair cells to AEP by first testing intact goldfish (Carassius auratus), then ablating their neuromasts with streptomycin sulphate-disabling superficial and canal neuromasts-and retesting the same goldfish. We performed a similar experiment where only the superficial neuromasts were physically ablated. At 100 and 200Hz, there was a 10-15?dB increase in threshold after streptomycin treatment but no significant difference at higher frequencies. There was no difference in threshold in control fish or in fish that only had superficial neuromasts removed, indicating that the differential responses were driven by canal neuromasts. Taken together, these results indicate that AEP results at lower frequencies should be interpreted as multimodal responses, rather than as \u27hearing\u27. The results also suggest that in natural situations both the ear and lateral line likely play an integrative role in detecting and localising many types of \u27acoustic\u27 stimuli. © 2013. Published by The Company of Biologists Ltd

Condition-dependent auditory processing in the round goby (Neogobius melanostomus): Links to sex, reproductive condition and female estrogen levels

Neural responses to sensory stimuli often differ between sexes, vary seasonally, and can be regulated by endocrine activity, but the ecological and physiological mechanisms driving such patterns are not well understood. The current study examined how auditory function in the round goby (Neogobius melanostomus), a vocal teleost, co-varied with sex, reproductive condition and female plasma 17β-estradiol level. Auditory evoked potentials were collected in response to tone pips (100–600Hz) and a natural round goby pulse vocalization. Additionally, saccule hair cell densities were compared across reproductive groups. Auditory threshold was evaluated in terms of pressure and particle acceleration, and response amplitude and onset latency were measured at 10dB above threshold. Relative to males, females displayed lower auditory thresholds in response to the natural vocalization and to tones at 300–600Hz, and had a higher density of saccule hair cells. The 17β-estradiol level was positively associated with amplitude and latency for the pulse stimulus and with both threshold and amplitude for tones at 100–200Hz in females. Relative to non-reproductive males, reproductive males exhibited longer response latencies at 100–200Hz. The results demonstrate sexual dimorphism in auditory function in a teleost fish as well as intra-sexual variation, partially based on hormone levels. The current research further identifies links between auditory function and reproductive behaviors in fishes and provides a finer-scaled analysis of how this behavior is reflected at the level of the sensory systems facilitating signal reception

Audition in sciaenid fishes with different swim bladder-inner ear configurations

We investigated how morphological differences in the auditory periphery of teleost fishes may relate to hearing capabilities. Two species of western Atlantic sciaenids were examined: weakfish (Cynoscion regalis, Block and Schneider) and spot (Leiostomus xanthurus, Lacepede). These species differ in the anatomical relationship between the swim bladder and the inner ear. In weakfish, the swim bladder has a pair of anterior horns that terminate close to the ear, while there are no extensions of the swim bladder in spot. Thus, the swim bladder in spot terminates at a greater distance from the ear when compared to weakfish. With the use of the auditory brainstem response technique, Cynoscion regalis were found to detect frequencies up to 2000 Hz, while Leiostomus xanthurus detected up to 700 Hz. There were, however, no significant interspecific differences in auditory sensitivity for stimuli between 200 and 700 Hz. These data support the hypothesis that the swim bladder can potentially expand the frequency range of detection

Field assessment of behavioural responses of southern stingrays (Hypanus americanus) to acoustic stimuli

The ability of elasmobranchs to detect and use sound cues has been heavily debated in previous research and has only recently received revived attention. To properly understand the importance of sound to elasmobranchs, assessing their responses to acoustic stimuli in a field setting is vital. Here, we establish a behavioural audiogram of free-swimming male and female southern stingrays (Hypanus americanus) exposed to low-frequency tones. We demonstrate that female stingrays exposed to tones (50-500 Hz) exhibit significant changes in swimming behaviours (increased time spent swimming, decreased rest time, increased surface breaches and increased side swimming with pectoral flapping) at 140 dB re 1 µPa (−2.08 to −2.40 dB re 1 m s−2) while males exposed to the same tones did not exhibit a change in these behaviours until 160 dB re 1 µPa (−1.13 to −1.21 dB re 1 m s−2). Our results are the first demonstration of field responses to sound in the Batoidea and show a distinct sensitivity to low-frequency acoustic inputs

Pressure and particle motion detection thresholds in fish: A re-examination of salient auditory cues in teleosts

The auditory evoked potential technique has been used for the past 30years to evaluate the hearing ability of fish. The resulting audiograms are typically presented in terms of sound pressure (dB re. 1Pa) with the particle motion (dB re. 1ms–2) component largely ignored until recently. When audiograms have been presented in terms of particle acceleration, one of two approaches has been used for stimulus characterisation: measuring the pressure gradient between two hydrophones or using accelerometers. With rare exceptions these values are presented from experiments using a speaker as the stimulus, thus making it impossible to truly separate the contribution of direct particle motion and pressure detection in the response. Here, we compared the particle acceleration and pressure auditory thresholds of three species of fish with differing hearing specialisations, goldfish (Carassius auratus, weberian ossicles), bigeye (Pempheris adspersus, ligamentous hearing specialisation) and a third species with no swim bladder, the common triplefin (Forstergyian lappillum), using three different methods of determining particle acceleration. In terms of particle acceleration, all three fish species have similar hearing thresholds, but when expressed as pressure thresholds goldfish are the most sensitive, followed by bigeye, with triplefin the least sensitive. It is suggested here that all fish have a similar ability to detect the particle motion component of the sound field and it is their ability to transduce the pressure component of the sound field to the inner ear via ancillary hearing structures that provides the differences in hearing ability. Therefore, care is needed in stimuli presentation and measurement when determining hearing ability of fish and when interpreting comparative hearing abilities between species

Behavioural and morphological changes in fish exposed to ecologically relevant boat noises

There is increasing concern about the effect of underwater noise on fish due to rising levels of anthropogenic noise. We performed experiments on the black bullhead (Ameiurus melas), a species with known hearing specializations and located within the Laurentian Great Lakes where there is considerable commercial and recreational boat traffic. We tested and compared physiology (baseline cortisol), behaviour (activity, sheltering), and morphology (ciliary bundles of hair cells) of bullhead to boat noise. At 140 dB re 1 μPa (−54.84 dB re 1 m·s−2), we saw clear behavioural effects in terms of both activity and sheltering levels despite no obvious morphological or physiological stress. Following both short-and long-period acute exposure to higher — but environmentally relevant — noise levels, bullhead were less active and sheltered more and also exhibited a decrease in ciliary bundles. These results suggest that there are sublethal effects of anthropogenic noise on fish behaviour and ciliary bundles, which may have direct implications on population health. Moreover, commonly used metrics such as stress hormones may not always offer the most relevant biomarker of the response to anthropogenic boat noise

Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio)

Investigations of the development of auditory form and function have, with a few exceptions, thus far been largely restricted to birds and mammals, making it difficult to postulate evolutionary hypotheses. Teleost fishes represent useful models for developmental investigations of the auditory system due to their often extensive period of posthatching development and the diversity of auditory specializations in this group. Using the auditory brainstem response and morphological techniques we investigated the development of auditory form and function in zebrafish ~Danio rerio) ranging in size from 10 to 45 mm total length. We found no difference in auditory sensitivity, response latency, or response amplitude with development, but we did find an expansion of maximum detectable frequency from 200 Hz at 10 mm to 4000 Hz at 45 mm TL. The expansion of frequency range coincided with the development of Weberian ossicles in zebrafish, suggesting that changes in hearing ability in this species are driven more by development of auxiliary specializations than by the ear itself. We propose a model for the development of zebrafish hearing wherein the Weberian ossicles gradually increase the range of frequencies available to the inner ear, much as middle ear development increases frequency range in mammals