Ecology of sound communication in fishes

Fishes communicate acoustically under ecological constraints which may modify or hinder signal transmission and detection and may also be risky. This makes it important to know if and to what degree fishes can modify acoustic signalling when key ecological factors—predation pressure, noise and ambient temperature—vary. This paper reviews short‐time effects of the first two factors; the third has been reviewed recently (Ladich, 2018 ). Numerous studies have investigated the effects of predators on fish behaviour, but only a few report changes in calling activity when hearing predator calls as demonstrated when fish responded to played‐back dolphin sounds. Furthermore, swimming sounds of schooling fish may affect predators. Our knowledge on adaptations to natural changes in ambient noise, for example caused by wind or migration between quiet and noisier habitats, is limited. Hearing abilities decrease when ambient noise levels increase (termed masking), in particular in taxa possessing enhanced hearing abilities. High natural and anthropogenic noise regimes, for example vessel noise, alter calling activity in the field and laboratory. Increases in sound pressure levels (Lombard effect) and altered temporal call patterns were also observed, but no switches to higher sound frequencies. In summary, effects of predator calls and noise on sound communication are described in fishes, yet sparsely in contrast to songbirds or whales. Major gaps in our knowledge on potential negative effects of noise on acoustic communication call for more detailed investigation because fishes are keystone species in many aquatic habitats and constitute a major source of protein for humans.     

Predator and prey events at the entrance of a surface-oriented fish collector at North Fork Dam,Oregon

Quantifiable estimates of predator–prey interactions and relationships in aquatic habitats are difficult to obtain and rare, especially when individuals cannot be readily observed. To overcome this observational impediment, imaging sonar was used to assess the cooccurrence of predator-size fish and juvenile salmonids, Oncorhynchus spp., at the entrance to a floating surface collector (FSC) in the forebay of North Fork Dam on the Clackamas River, Oregon (USA). Imaging sonar can be used to transform active sound waves into visual data, making it possible to obtain continuous underwater observations on the presence and interspecific interactions between predator-size fish and prey (juvenile salmonids). Hourly counts of smolt-size fish tracks, diel phase, water clarity and river discharge were used as covariates within a zero-inflated Poisson model to determine how these factors may influence the number of predators in front of the FSC. Both the number of smolt-size fish tracks and diel phase had the strongest effects on the number of predator-size fish tracks, with more predator-size fish tracks observed during the daytime, and as the number of smolt-size fish tracks increased. Additionally, the presence of predator-size fish may affect the abundance and direction of travel of juvenile salmonids, as fewer smolt-size fish were observed when predators were present, and a greater proportion of smolt-size fish were observed travelling away from the FSC when predator-size fish were present. This study provides estimates of predator and prey fish abundance in the vicinity of surface collection systems at moderate-sized hydropower projects and could help resource managers better understand mechanisms that can influence the survival and passage behaviour of juvenile salmonids using surface collection structures at dams.     

Foraging arena theory

There is a critical need for quantitative models that can help evaluate trade‐off decisions related to the impacts of harvesting and protection of aquatic ecosystems within an ecosystem context. Ecosystem models used to evaluate such trade‐offs need to have the capability of capturing the dynamic stability that can arise when predator‐prey interactions are restricted to spatial and temporal arenas. Foraging arenas appear common in aquatic systems and are created by a wide range of mechanisms, ranging from restrictions of predator distributions in response to predation risk caused by their own predators, to risk‐sensitive foraging behaviour by their prey. Foraging arenas partition the prey in each predator‐prey interaction in a food web into vulnerable and invulnerable states, with exchange between these states potentially limiting overall trophic flow. Inclusion of vulnerability exchange processes in models for recruitment processes and food web responses to disturbances like harvesting leads to very different predictions about dynamic stability, trophic cascades and maintenance of ecological diversity than do models based on large‐scale mass action (random mixing) interactions between prey and predators. Although a number of methods to estimate these critical exchange rates are presented, none are considered fully satisfactory. The most important challenge for the practical application of models that incorporate foraging arena theory today is not only developing new or improved methods for measuring exchange rates but also evaluating how such rates vary in responses to major fishery‐induced changes in abundances of predators.     

Size-dependent predation on marine fish larvae by Ctenophores, Scyphomedusae, and Planktivorous fish

Size-dependent predation rates on marine fish larvae by the ctenophore Mnemiopsis leidyi , scyphomedusa Chrysaora quinquecirrha , and planktivorous fish Anchoa mitchilli were estimated via experiments in 3.2 m³ me-socosms. Predation rates on larvae of the goby Gobio-soma bosci were estimated in relation to 1) length of larval prey, 2) presence or absence of alternative < 1 mm zooplankton prey, and 3) a predator-prey interaction between the scyphomedusa and ctenophore. The consumption rate of larvae by the three predators generally declined as larval length increased. The ctenophore ate fewer (1.0 d^-1 per predator) larvae than did the medusa (7.8 d ^-1 per predator) or bay anchovy (4.0 d ^-1 per predator), but it consumed larvae in all size classes tested (3.0–9.5 mm SL). Predation by bay anchovy and the medusa was more size-dependent: 3.0–5.0 mm larvae were most vulnerable. Fewer larvae were eaten by the ctenophore and bay anchovy when zooplankton alternative prey was available, but predation on larvae by the medusa was not influenced by alternative zooplankton prey. Consumption rate of fish larvae by the medusa was reduced 20–25% when the ctenophore was present as its alternative prey. An encounter-rate model was developed and its parameters estimated from the experimental results. Model simulations indicated that the relationship between larval size and vulnerability is dependent on size, swimming speed, and behavior of both predators and larvae, and that bigger or faster-growing fish larvae are not always less vulnerable to predation.     

Turbidity‐induced changes in emergent effects of multiple predators with different foraging strategies

Abstract – In natural systems, prey frequently interact with multiple predators and the outcome often cannot be predicted by summing the effects of individual predator species. Multiple predator interactions can create emergent effects for prey, but how those change across environmental gradients is poorly understood. Turbidity is an environmental factor in aquatic systems that may influence multiple predator effects on prey. Interactions between a cruising predator (largemouth bass Micropterus salmoides) and an ambush predator (muskellunge Esox masquinongy) and their combination foraging on a shared prey (bluegill Lepomis macrochirus) were examined across a turbidity gradient. Turbidity modified multiple predator effects on prey. In clear water, combined predators consumed in total more prey than expected from individual predator treatments, suggesting risk enhancement for prey. In moderately turbid water, the predators consumed fewer prey together than expected, suggesting a risk reduction for prey. At high turbidity, there were no apparent emergent effects; however, the cruising predator consumed more prey than the ambush predator, suggesting an advantage for this predator. Understanding multiple predator traits across a gradient of turbidity increases our understanding of how complex natural systems function.     

A meta‐analysis of fish behavioural reaction to underwater human presence

In an increasingly anthropic world, humans have profound impacts on the distribution and behaviour of marine fishes. The increased human presence has modified fishes’ antipredator behavioural responses, and consequently flight decisions, as a function of their changed perceptions of risk. Understanding how fish react to human presence can help identify the most vulnerable functional groups/species and estimate impacts caused by human disturbance. Shoal and body size are known to influence fish flight initiation distance (FID; the distance between the predator and prey when the prey begins to escape); however, few studies attempt to test the moderators of these relationships. Here, we present a comprehensive meta‐analysis evaluating FID of fish in response to human presence. Specifically, we investigated six candidate moderators that could influence the relationship between FID with shoal and body size. Our results showed that individual fish size was strongly and positively correlated with FID and the most important moderator that explained the variance in individual body size‐FID relationship was shoaling behaviour. However, and somehow surprisingly, we detected no significant relationship between shoal size and FID. We discuss how these results can inform the development of fish conservation strategies and ultimately assist in the management of marine protected areas.     

An individual based model of fish school reactions: predicting antipredator behaviour as observed in nature

An object-orientated, two-dimensional, cellular automata (CA) model is developed to describe and predict the schooling behaviour of fish in general, with Norwegian spring-spawning herring, Clupea harengus L., being used as a case study. The CA model is applied to visualize internal school dynamics based on individual decision rules. Several antipredator strategies, such as split , join and vacuole, performed by schools during predator attack, are visualized in the model. The primary driving force of individual fish is based on simple attraction rules. The model includes stochastic elements which assume that individual herring do not have perfect information about their surroundings. Isolation of individual fish from a school during predator attack is also predicted by the model. The disruption of highly organized fish schools, followed by an attack on solitary herring individuals, may be an important tactic for predators feeding on schooling prey. The conceptual CA model identifies patterns and mechanisms both within and between schools that may be important in all schooling fish. Model simulations are compared with observed predator–prey interactions between killer whales, Orcinus orca L., and herring in northern Norway.     

Effects of ambient acidity on chemosensory learning: an example of an environmental constraint on acquired predator recognition in wild juvenile Atlantic salmon (Salmo salar)

Abstract –  In many prey fish species, learning the identity of novel predators may be facilitated when novel predator cues and an aversive stimulus are presented together. Damage-released chemical alarm cues are typically released from the skin of prey individuals following mechanical damage and are known to mediate the learned recognition of novel predators. While such chemically mediated acquired predator recognition can provide increased survival benefits to prey, environmental constraints impeding learning may exist. For example, in several fish species the ability to detect chemical alarm cues is impaired in under acidic conditions and as such, inhibits this chemically mediated learning. In this experiment, we studied in two streams of different mean acidity level (pH c . 6.0 and 7.0), to assess if wild juvenile Atlantic salmon ( Salmo salar ) had the ability to acquire the recognition of a novel lemon essence odour when paired with conspecific chemical alarm cues. Our results demonstrate that under acidic conditions, no learned recognition of the novel odour occurred. In neutral conditions, however, salmon recognised the novel odour as a predation threat. This result suggests that ambient acidity creates an environmental constraint on chemically mediated learned recognition of a novel cue.     

Instream cover and shade mediate avian predation on trout in semi‐natural streams

Piscivory by birds can be significant, particularly on fish in small streams and during seasonal low flow when available cover from predators can be limited. Yet, how varying amounts of cover may change the extent of predation mortality from avian predators on fish is not clear. We evaluated size‐selective survival of coastal cutthroat trout (Oncorhynchus clarkii clarkii) in replicated semi‐natural stream sections. These sections provided high (0.01 m² of cover per m² of stream) or low (0.002 m² of cover per m² of stream) levels of instream cover available to trout and were closed to emigration. Each fish was individually tagged, allowing us to track retention of individuals during the course of the 36‐day experiment, which we attributed to survival from predators, because fish had no other way to leave the streams. Although other avian predators may have been active in our system and not detected, the only predator observed was the belted kingfisher Megaceryle alcyon, which is known to prey heavily on fish. In both treatments, trout >20.4 cm were not preyed upon indicating an increased ability to prey upon on smaller individuals. Increased availability of cover improved survival of trout by 12% in high relative to low cover stream sections. Trout also survived better in stream sections with greater shade, a factor we could not control in our system. Collectively, these findings indicate that instream cover and shade from avian predators can play an important role in driving survival of fish in small streams or during periods of low flow.     

Population‐level consequences of seismic surveys on fishes: An interdisciplinary challenge

Offshore activities elevate ambient sound levels at sea, which may affect marine fauna. We reviewed the literature about impact of airgun acoustic exposure on fish in terms of damage, disturbance and detection and explored the nature of impact assessment at population level. We provided a conceptual framework for how to address this interdisciplinary challenge, and we listed potential tools for investigation. We focused on limitations in data currently available, and we stressed the potential benefits from cross‐species comparisons. Well‐replicated and controlled studies do not exist for hearing thresholds and dose–response curves for airgun acoustic exposure. We especially lack insight into behavioural changes for free‐ranging fish to actual seismic surveys and on lasting effects of behavioural changes in terms of time and energy budgets, missed feeding or mating opportunities, decreased performance in predator‐prey interactions, and chronic stress effects on growth, development and reproduction. We also lack insight into whether any of these effects could have population‐level consequences. General “population consequences of acoustic disturbance” (PCAD) models have been developed for marine mammals, but there has been little progress so far in other taxa. The acoustic world of fishes is quite different from human perception and imagination as fish perceive particle motion and sound pressure. Progress is therefore also required in understanding the nature and extent to which fishes extract acoustic information from their environment. We addressed the challenges and opportunities for upscaling individual impact to the population, community and ecosystem level and provided a guide to critical gaps in our knowledge.     

Possible functions of the octavolateralis system in fish schooling

The development of the octavolateralis system in fish ancestors created the phenomenon of sensory reafference associated with the fish's own locomotion. Particularly in fish species living and moving in groups, there is a potential to produce complex pressure waves and other water movements interfering with the octavolateralis perception of critical environmental signals. The hypothesis presented is that the development of the octavolateralis system may have initiated, or been a factor in, the evolutionary development of synchronized group locomotion, eventually leading to schooling behaviour. Theoretical models suggest that schooling may be related to a reduction in masking of environmental signals, as well as to survival mechanisms, e.g. confusion of the lateral line and electro-sensory systems of predators by overlapping pressure waves and overlapping electrical fields. The combined effects of reduced masking and predator confusion may help explain why schooling became an evolutionary success. Including pressure waves and other water movements in the model of join, stay or leave decisions might shed some light on fish shoal assortment. A model encompassing the complex effects of synchronized group locomotion on octavolateralis and electro-sensory perception of both prey and predator fish might increase the understanding of schooling behaviour.     

Individual feeding specialisation of a naïve vs. veteran predators

Abstract – We explored the incidence of individual feeding specialisation among a naïve predator (non‐native rainbow trout postsmolts) and two native experienced predators (sea‐run Arctic charr and sea‐trout) in a subarctic Norwegian fjord. Interindividual foraging niche stability was obtained by combining information on stomach contents (recent dietary niche) with trophically transmitted parasite infestation (time‐integrated historical dietary niche) of individual predators. Individual fish showed a high degree of resource specialisation as prey items such as gammarids and small fish (both potential intermediate host of parasites) rarely co‐occurred in stomachs. In both naïve and veteran predators, positive associations between the intensity of a specific parasite species and the occurrence of their respective intermediate host (gammarids or fish) in the stomachs of individual predators demonstrated temporally interindividual feeding specialisations. Several behavioural phenotypes clearly co‐existed in both naïve and veteran predator populations, including gammaridivore (benthic feeders), piscivore (pelagic feeders) or insectivore (pleuston feeders) individuals. The likely mechanism of this observed interindividual resource specialisation in the non‐native naïve predators involves a behavioural component of which rapid learning seems to be a key factor.     

草鱼敏感的负趋音筛选研究

声学屏障是一种阻拦鱼类进入危险区域进而保护鱼类资源的重要手段,为筛选鱼类敏感的负趋音作为声学屏障,本文采用六种单频音（500-3 000 Hz）和一种宽频音（短吻鳄吼叫声）作为实验用音对草鱼幼鱼进行负趋音的筛选研究,通过在水槽两端交替播音来对比草鱼幼鱼对不同声音的行为反应。结果表明,大多数实验鱼对声音有反应,短吻鳄吼叫声与其他声音组的差异显著。单频音实验组中播放500 Hz单频音时平均反应次数最大,为1.7±0.6次,而播放短吻鳄吼叫声时平均反应次数高达5±0.9次,显著高于其他实验音;在总平均速度中,宽频音组中草鱼的总平均速度显著高于其他组,表明草鱼对短吻鳄吼叫声敏感,产生逃窜行为。本研究表明,草鱼对短吻鳄吼叫声具有负趋音性,短吻鳄吼叫声可能是一种对草鱼具有驱赶、威慑作用的声音,本研究可为过鱼设施中辅助诱驱鱼手段及水利结构中避免鱼类的夹带提供参考依据。     

Potential direct and indirect effects of climate change on a shallow natural lake fish assemblage

Much uncertainty exists around how fish communities in shallow lakes will respond to climate change. In this study, we modelled the effects of increased water temperatures on consumption and growth rates of two piscivores (northern pike [Esox lucius] and largemouth bass [Micropterus salmoides]) and examined relative effects of consumption by these predators on two prey species (bluegill [Lepomis macrochirus] and yellow perch [Perca flavescens]). Bioenergetics models were used to simulate the effects of climate change on growth and food consumption using predicted 2040 and 2060 temperatures in a shallow Nebraska Sandhill lake, USA. The patterns and magnitude of daily and cumulative consumption during the growing season (April–October) were generally similar between the two predators. However, growth of northern pike was always reduced (?3 to ?45% change) compared to largemouth bass that experienced subtle changes (4 to ?6% change) in weight by the end of the growing season. Assuming similar population size structure and numbers of predators in 2040–2060, future consumption of bluegill and yellow perch by northern pike and largemouth bass will likely increase (range: 3–24%), necessitating greater prey biomass to meet future energy demands. The timing of increased predator consumption will likely shift towards spring and fall (compared to summer), when prey species may not be available in the quantities required. Our findings suggest that increased water temperatures may affect species at the edge of their native range (i.e. northern pike) and a potential mismatch between predator and prey could exist.     

Acoustic communication in fishes: Temperature plays a role

Temperature affects peripheral and central mechanisms of signal production and detection in ectothermic animals. This study reviews for the first time the effects of temperature on acoustic communication in fishes and analyses whether changes in sound properties are coupled to changes in auditory sensitivities. Effects of temperature on sound production have been studied in approximately one dozen families of teleosts. Calling activity increased or was unaffected by temperature, in the latter case probably because seasonal, daily and lunar rhythms also influence mating behaviour and calling. Sound characteristics (pulse repetition rate, fundamental frequency) are positively correlated with temperature if pulses are directly based on sonic muscle contractions. In fishes possessing other sonic mechanisms, the dominant frequency of their pulsatile pectoral sounds may increase as well. Auditory sensitivities were mainly determined in otophysines, which possess enhanced hearing abilities. Studies revealed that hearing increased with temperature, in particular at higher frequencies. We know close to nothing about whether temperature‐dependent changes in sound characteristics are coupled to changes in auditory sensitivity or mate choice. Female midshipman toadfish appear to choose males based on call frequency, which varies with temperature. Future studies need to address several topics: (i) temperature effects on sound production have to be separated from other sources of variation; (ii) effects on hearing need to be studied in many more taxa; (iii) potential negative effects of global warming on acoustic communication (because of temperature coupling) need to be investigated because fish constitute a major source of protein for humans.     

草鱼敏感的负趋音筛选

声学屏障是一种阻拦鱼类进入危险区域进而保护鱼类资源的重要手段,为筛选鱼类敏感的负趋音作为声学屏障,本研究采用6种单频音 (500~3 000 Hz)和1种宽频音 (扬子鳄吼叫声)作为实验用音对草鱼幼鱼进行负趋音的筛选研究,通过在水槽两端交替播音来对比草鱼幼鱼对不同声音的行为反应。结果显示,大多数实验鱼对声音有反应,扬子鳄吼叫声与其他声音组的差异显著。单频音实验组中播放500 Hz单频音时平均反应次数最大,为 (1.7±0.6)次,而播放扬子鳄吼叫声时平均反应次数高达 (5.0±0.9)次,显著高于其他实验音。在总平均速度中,宽频音组中草鱼的总平均速度显著高于其他组,表明草鱼对扬子鳄吼叫声敏感,产生逃窜行为。研究表明,草鱼对扬子鳄吼叫声具有负趋音性,扬子鳄吼叫声是一种对草鱼具有驱赶、威慑作用的声音。本研究可为过鱼设施中辅助诱驱鱼手段及水利结构中避免鱼类的夹带提供参考依据。     

Differentiated predation risk on hatchery-reared juvenile masu salmon by white-spotted charr with different body sizes

Predation after release is one of the major concerns of hatchery fish propagation. However, size-specific interaction between predator and prey on the survival of hatchery-released salmonid fish is largely unknown. To understand the size-selective predation risk, 24-h predation experiments were conducted on masu salmon Oncorhynchus masou in tanks. Four ranges of fork length (FL) were examined for masu salmon as a prey, in combination with three ranges of FL for white-spotted charr Salvelinus leucomaenis as a predator. The results show that not only predator and prey sizes, but also interaction between prey size and predator size, strongly affected the survival rate of masu salmon. Predation on masu salmon with the FL exceeding 40% of the FL of white-spotted charr was rare in the experiment. A logistic regression suggests that 37% relative FL of masu salmon to white-spotted charr results in the 50% survival of masu salmon. Our results suggest that adjusting relative size of hatchery fish to the size of local fish predators at the time of hatchery release will have a significant impact on the survival of hatchery fish in the wild. From this perspective, site-specific, adaptive management might be important to improve the effectiveness of hatchery fish propagation.     

Ecological processes influencing mortality of juvenile pink salmon (Oncorhynchus gorbuscha) in Prince William Sound,Alaska

Our collaborative work focused on understanding the system of mechanisms influencing the mortality of juvenile pink salmon (Oncorhynchus gorbuscha) in Prince William Sound, Alaska. Coordinated field studies, data analysis and numerical modelling projects were used to identify and explain the mechanisms and their roles in juvenile mortality. In particular, project studies addressed the identification of major fish and bird predators consuming juvenile salmon and the evaluation of three hypotheses linking these losses to (i) alternative prey for predators (prey‐switching hypothesis); (ii) salmon foraging behaviour (refuge‐dispersion hypothesis); and (iii) salmon size and growth (size‐refuge hypothesis). Two facultative planktivorous fishes, Pacific herring (Clupea pallasi) and walleye pollock (Theragra chalcogramma), probably consumed the most juvenile pink salmon each year, although other gadids were also important. Our prey‐switching hypothesis was supported by data indicating that herring and pollock switched to alternative nekton prey, including juvenile salmon, when the biomass of large copepods declined below about 0.2 g m^?3. Model simulations were consistent with these findings, but simulations suggested that a June pteropod bloom also sheltered juvenile salmon from predation. Our refuge‐dispersion hypothesis was supported by data indicating a five‐fold increase in predation losses of juvenile salmon when salmon dispersed from nearshore habitats as the biomass of large copepods declined. Our size‐refuge hypothesis was supported by data indicating that size‐ and growth‐dependent vulnerabilities of salmon to predators were a function of predator and prey sizes and the timing of predation events. Our model simulations offered support for the efficacy of representing ecological processes affecting juvenile fishes as systems of coupled evolution equations representing both spatial distribution and physiological status. Simulations wherein model dimensionality was limited through construction of composite trophic groups reproduced the dominant patterns in salmon survival data. In our study, these composite trophic groups were six key zooplankton taxonomic groups, two categories of adult pelagic fishes, and from six to 12 groups for tagged hatchery‐reared juvenile salmon. Model simulations also suggested the importance of salmon density and predator size as important factors modifying the predation process.     

Habitat use of lake trout (Salvelinus namaycush) following species introduction

Abstract – Although introductions of prey species have the potential to significantly alter habitat use by top predatory fish, this aspect has rarely been directly quantified. Introduction of yellow perch (Perca flavescens), a littoral–pelagic prey species, to a small boreal lake previously dominated by littoral cyprinids provided a unique opportunity to examine how a change in forage base influenced habitat use by the sole top predator, lake trout (Salvelinus namaycush). We monitored lake trout pelagic and spatial distribution using acoustic telemetry before (2001) and after (2008) the introduction of perch to determine whether habitat use reflected a deeper, offshore prey community. After accounting for differences in water temperature and dissolved oxygen concentrations between years and the inclusion of a control lake, our data suggest that lake trout habitat use changed after the introduction of yellow perch. Lake trout, on average, were 1.4 m deeper (P < 0.01), reduced their use of littoral habitat by 55% (P = 0.03) and experienced a 71% decrease in home range size (P < 0.01), consistent with a greater offshore habitat overlap between predator and prey after the introduction of yellow perch. This study illustrates how introduced prey species may have a significant influence on habitat use by top predatory fish, while also showing the importance of using direct measurements to quantify behavioural changes.     

Learning of foraging skills by fish

This chapter outlines the relationships between a number of key factors that influence learning and memory, and illustrates them by reference to studies on the foraging behaviour of fish. Learning can lead to significant improvements in foraging performance in only a few exposures, and at least some fish species are capable of adjusting their foraging strategy as patterns of patch profitability change. There is also evidence that the memory window for prey varies between fish species, and that this may be a function of environmental predictability. Convergence between behavioural ecology and comparative psychology offers promise in terms of developing more mechanistically realistic foraging models and explaining apparently ‘suboptimal’ patterns of behaviour. Foraging decisions involve the interplay between several distinct systems of learning and memory, including those that relate to habitat, food patches, prey types, conspecifics and predators. Fish biologists, therefore, face an interesting challenge in developing integrated accounts of fish foraging that explain how cognitive sophistication can help individual animals to deal with the complexity of the ecological context.