Anthropogenic underwater vibrations are sensed and stressful for the shore crab Carcinus maenas.

Acoustic pollution in aquatic environments has increased with adverse effects on many aquatic organisms. However, little work has been done considering the effects of the vibratory component of acoustic stimuli, which can be transmitted in the substrate and propagated into the aquatic medium. Benthic marine organisms, including many invertebrates, are capable of sensing seabed vibration, yet the responses they trigger on organism have received little attention. This study investigates the impact of underwater vibration on the physiology and behaviour of a ubiquitous inhabitant of coastal areas of the northern hemisphere, the shore crab Carcinus maenas. We developed a novel vibratory apparatus with geophones supported on a softly sprung frame to induce a seabed vibration of 20 Hz frequency, as observed during dredging, piling and other anthropogenic activities. The geophone internal mass caused the frame to vibrate in a controlled manner. Our results show that transition from ambient to anthropogenic vibrations induced an increase in activity and antennae beats in shore crabs, indicating perception of the vibratory stimulus and a higher stress level. There was also a trend on sex-specific responses to anthropogenic vibration, with males showing a higher activity level than females. However, no effect of anthropogenic vibrations was found upon oxygen consumption. These results show that anthropogenic underwater vibration induces behavioural responses in Carcinus maenas. This highlights the importance of evaluating man-made vibratory activities on coastal invertebrates and the necessity of evaluating anthropogenic effects on both sexes.

Anthropogenic noise pollution from pile-driving disrupts the structure and dynamics of fish shoals.

Noise produced from a variety of human activities can affect the physiology and behaviour of individual animals, but whether noise disrupts the social behaviour of animals is largely unknown. Animal groups such as flocks of birds or shoals of fish use simple interaction rules to coordinate their movements with near neighbours. In turn, this coordination allows individuals to gain the benefits of group living such as reduced predation risk and social information exchange. Noise could change how individuals interact in groups if noise is perceived as a threat, or if it masked, distracted or stressed individuals, and this could have impacts on the benefits of grouping. Here, we recorded trajectories of individual juvenile seabass (Dicentrarchus labrax) in groups under controlled laboratory conditions. Groups were exposed to playbacks of either ambient background sound recorded in their natural habitat, or playbacks of pile-driving, commonly used in marine construction. The pile-driving playback affected the structure and dynamics of the fish shoals significantly more than the ambient-sound playback. Compared to the ambient-sound playback, groups experiencing the pile-driving playback became less cohesive, less directionally ordered, and were less correlated in speed and directional changes. In effect, the additional-noise treatment disrupted the abilities of individuals to coordinate their movements with one another. Our work highlights the potential for noise pollution from pile-driving to disrupt the collective dynamics of fish shoals, which could have implications for the functional benefits of a group's collective behaviour.

Expanding the Link between Out-Group Threats and In-Group Behavior: (A Reply to Kavaliers and Choleris).

In social species, groups and their members face a variety of threats from conspecific outsiders. Such out-group conflict is predicted to influence within-group behavior, with empirical work demonstrating this link in humans, primates, and birds. In our note "Out-Group Threat Promotes Within-Group Affiliation in a Cooperative Fish," appearing in The American Naturalist in February 2016, we provided experimental evidence that simulated territorial intrusions result in subsequent increases in affiliation among groupmates in a cichlid fish (Neolamprologus pulcher). Martin Kavaliers and Elena Choleris, in their comment "Out-Group Threat Responses, In-Group Bias, and Nonapeptide Involvement Are Conserved Across Vertebrates," appearing in this issue, commented on our cichlid-fish article; they consider the conserved nature of the link between out-group threat and in-group behavior and bias in vertebrates, the influence of pathogens in the process, and the potential underpinning hormonal mechanisms. Here, we provide clarification and expansion of some of the core points that are discussed in the comment by Kavaliers and Choleris.

Shipbuilding Docks as Experimental Systems for Realistic Assessments of Anthropogenic Stressors on Marine Organisms.

Empirical investigations of the impacts of anthropogenic stressors on marine organisms are typically performed under controlled laboratory conditions, onshore mesocosms, or via offshore experiments with realistic (but uncontrolled) environmental variation. These approaches have merits, but onshore setups are generally small sized and fail to recreate natural stressor fields, whereas offshore studies are often compromised by confounding factors. We suggest the use of flooded shipbuilding docks to allow studying realistic exposure to stressors and their impacts on the intra- and interspecific responses of animals. Shipbuilding docks permit the careful study of groups of known animals, including the evaluation of their behavioral interactions, while enabling full control of the stressor and many environmental conditions. We propose that this approach could be used for assessing the impacts of prominent anthropogenic stressors, including chemicals, ocean warming, and sound. Results from shipbuilding-dock studies could allow improved parameterization of predictive models relating to the environmental risks and population consequences of anthropogenic stressors.

Rapid recovery following short-term acoustic disturbance in two fish species.

Noise from human activities is known to impact organisms in a variety of taxa, but most experimental studies on the behavioural effects of noise have focused on examining responses associated with the period of actual exposure. Unlike most pollutants, acoustic noise is generally short-lived, usually dissipating quickly after the source is turned off or leaves the area. In a series of experiments, we use established experimental paradigms to examine how fish behaviour and physiology are affected, both during short-term (2 min) exposure to playback of recordings of anthropogenic noise sources and in the immediate aftermath of noise exposure. We considered the anti-predator response and ventilation rate of juvenile European eels (Anguilla anguilla) and ventilation rate of juvenile European seabass (Dicentrarchus labrax). As previously found, additional-noise exposure decreased eel anti-predator responses, increased startle latency and increased ventilation rate relative to ambient-noise-exposed controls. Our results show for the first time that those effects quickly dissipated; eels showed rapid recovery of startle responses and startle latency, and rapid albeit incomplete recovery of ventilation rate in the 2 min after noise cessation. Seabass in both laboratory and open-water conditions showed an increased ventilation rate during playback of additional noise compared with ambient conditions. However, within 2 min of noise cessation, ventilation rate showed complete recovery to levels equivalent to ambient-exposed control individuals. Care should be taken in generalizing these rapid-recovery results, as individuals might have accrued other costs during noise exposure and other species might show different recovery times. Nonetheless, our results from two different fish species provide tentative cause for optimism with respect to recovery following short-duration noise exposure, and suggest that considering periods following noise exposures could be important for mitigation and management decisions.

Out-Group Threat Promotes Within-Group Affiliation in a Cooperative Fish.

In social species, conflict with outsiders is predicted to affect within-group interactions and thus influence group dynamics and the evolution and maintenance of sociality. Although empirical evidence exists for a relationship between out-group conflict and intragroup behavior in humans, experimental tests in other animals are rare. In a model fish system, we show that simulated out-group intrusions cause postconflict increases in intragroup affiliation but no changes in postconflict intragroup aggression. Postconflict affiliation was greater following intrusions by neighboring compared with nonneighboring individuals; neighbors represent greater threats to the dominance rank and breeding success of residents, and they are visible in the aftermath of the intrusion. By providing strong evidence of a link between out-group conflict and postconflict intragroup behavior and demonstrating that intragroup affiliation is affected by the nature of the out-group intrusion, our study shows the importance of considering postconflict behavior for our understanding of cooperation and social structure.

Condition-dependent physiological and behavioural responses to anthropogenic noise.

Anthropogenic (man-made) noise, a global pollutant of international concern, is known to affect the physiology and behaviour of a range of organisms. However, experimental studies have tended to focus on trait means; intra-population variation in responses are likely, but have rarely been explored. Here we use established experimental methods to demonstrate a condition-dependent effect of additional noise. We show that juvenile European eels (Anguilla anguilla) in good condition do not respond differently to playbacks of ambient coastal noise and coastal noise with passing ships. By contrast, the additional noise of ship passes caused an increase in ventilation rate and a decrease in startling to a looming predatory stimulus in poor condition eels. Intra-population variation in responses to noise has important implications both for population dynamics and the planning of mitigation measures.

Beyond a Simple Effect: Variable and Changing Responses to Anthropogenic Noise.

A growing number of experimental studies have demonstrated that exposure to anthropogenic noise can affect the behavior and physiology of a variety of aquatic organisms. However, work in other fields suggests that responses are likely to differ between species, individuals, and situations and across time. We suggest that issues such as interspecific and intrapopulation variation, context dependency, repeated exposure and prior experience, and recovery and compensation need to be considered if we are to gain a full understanding of the impacts of this global pollutant.

Chronic playback of boat noise does not impact hatching success or post-hatching larval growth and survival in a cichlid fish.

Anthropogenic (man-made) noise has been shown to have a negative impact on the behaviour and physiology of a range of terrestrial and aquatic animals. However, direct assessments of fitness consequences are rare. Here we examine the effect of additional noise on early life stages in the model cichlid fish, Neolamprologus pulcher. Many fishes use and produce sounds, they are crucial elements of aquatic ecosystems, and there is mounting evidence that they are vulnerable to anthropogenic noise; adult N. pulcher have recently been shown to change key behaviours during playback of motor boat noise. Using a split-brood design to eliminate potential genetic effects, we exposed half of the eggs and fry from each clutch to four weeks of playbacks of noise originally recorded from small motor boats with the other half acting as a control (receiving no noise playback). There was no significant effect of additional noise on hatching success or fry survival, length or weight at the end of the exposure period. Although care should be taken not to generalize these findings on a single species from a laboratory study, our data suggest that moderate noise increases do not necessarily have direct negative impacts on early-life survival and growth. Further studies on a range of species in natural conditions are urgently needed to inform conservation efforts and policy decisions about the consequences of anthropogenic noise.

Intra- and interspecific challenges modulate cortisol but not androgen levels in a year-round territorial damselfish.

Interactions between individuals of different species are commonplace in animal communities. Some behaviors displayed during these interspecific social interactions may be very similar to those displayed during intraspecific social interactions. However, whether functional analogies between intra- and interspecific behaviors translate at the proximate level into an overlap in their underlying endocrine mechanisms remains largely unknown. Because steroids both mediate social behaviors and respond to them, we approached this question by comparing the behavioral and steroid response of free-living dusky gregories (Stegastes nigricans) to standardized territorial intrusions (sTI) of either conspecific or heterospecific food competitors. Stegastes nigricans is a year-round territorial fish that 'cultivates' the algae on which it feeds and is highly aggressive to both intra- and interspecific intruders. Behavioral differences between intra- and interspecific aggressive responses to sTI were marginal, and sTI tests caused an increase in cortisol levels that was positively related with the levels of aggression. In contrast, androgen levels did not increase in response to sTI, yet they showed a positive relationship with agonistic behavior. These results parallel a pattern that was first described for year-round territorial bird species. Furthermore, they suggest that changes in endocrine-hormone levels during territoriality might be independent of the species that induces the territorial response.

Paternity of subordinates raises cooperative effort in cichlids.

BACKGROUND: In cooperative breeders, subordinates generally help a dominant breeding pair to raise offspring. Parentage studies have shown that in several species subordinates can participate in reproduction. This suggests an important role of direct fitness benefits for cooperation, particularly where groups contain unrelated subordinates. In this situation parentage should influence levels of cooperation. Here we combine parentage analyses and detailed behavioural observations in the field to study whether in the highly social cichlid Neolamprologus pulcher subordinates participate in reproduction and if so, whether and how this affects their cooperative care, controlling for the effect of kinship. METHODOLOGY/PRINCIPAL FINDINGS: We show that: (i) male subordinates gained paternity in 27.8% of all clutches and (ii) if they participated in reproduction, they sired on average 11.8% of young. Subordinate males sharing in reproduction showed more defence against experimentally presented egg predators compared to subordinates not participating in reproduction, and they tended to stay closer to the breeding shelter. No effects of relatedness between subordinates and dominants (to mid-parent, dominant female or dominant male) were detected on parentage and on helping behaviour. CONCLUSIONS/SIGNIFICANCE: This is the first evidence in a cooperatively breeding fish species that the helping effort of male subordinates may depend on obtained paternity, which stresses the need to consider direct fitness benefits in evolutionary studies of helping behaviour.