Context-dependent multimodal behaviour in a coral reef fish.

Animals are expected to respond flexibly to changing circumstances, with multimodal signalling providing potential plasticity in social interactions. While numerous studies have documented context-dependent behavioural trade-offs in terrestrial species, far less work has considered such decision-making in fish, especially in natural conditions. Coral reef ecosystems host 25% of all known marine species, making them hotbeds of competition and predation. We conducted experiments with wild Ambon damselfish (Pomacentrus amboinensis) to investigate context-dependent responses to a conspecific intruder; specifically, how nest defence is influenced by an elevated predation risk. We found that nest-defending male Ambon damselfish responded aggressively to a conspecific intruder, spending less time sheltering and more time interacting, as well as signalling both visually and acoustically. In the presence of a model predator compared to a model herbivore, males spent less time interacting with the intruder, with a tendency towards reduced investment in visual displays compensated for by an increase in acoustic signalling instead. We therefore provide ecologically valid evidence that the context experienced by an individual can affect its behavioural responses and multimodal displays towards conspecific threats.

A shark's eye view: testing the 'mistaken identity theory' behind shark bites on humans.

Shark bites on humans are rare but are sufficiently frequent to generate substantial public concern, which typically leads to measures to reduce their frequency. Unfortunately, we understand little about why sharks bite humans. One theory for bites occurring at the surface, e.g. on surfers, is that of mistaken identity, whereby sharks mistake humans for their typical prey (pinnipeds in the case of white sharks). This study tests the mistaken identity theory by comparing video footage of pinnipeds, humans swimming and humans paddling surfboards, from the perspective of a white shark viewing these objects from below. Videos were processed to reflect how a shark's retina would detect the visual motion and shape cues. Motion cues of humans swimming, humans paddling surfboards and pinnipeds swimming did not differ significantly. The shape of paddled surfboards and human swimmers was also similar to that of pinnipeds with their flippers abducted. The difference in shape between pinnipeds with abducted versus adducted flippers was bigger than between pinnipeds with flippers abducted and surfboards or human swimmers. From the perspective of a white shark, therefore, neither visual motion nor shape cues allow an unequivocal visual distinction between pinnipeds and humans, supporting the mistaken identity theory behind some bites.

The soundscape of the Anthropocene ocean.

Oceans have become substantially noisier since the Industrial Revolution. Shipping, resource exploration, and infrastructure development have increased the anthrophony (sounds generated by human activities), whereas the biophony (sounds of biological origin) has been reduced by hunting, fishing, and habitat degradation. Climate change is affecting geophony (abiotic, natural sounds). Existing evidence shows that anthrophony affects marine animals at multiple levels, including their behavior, physiology, and, in extreme cases, survival. This should prompt management actions to deploy existing solutions to reduce noise levels in the ocean, thereby allowing marine animals to reestablish their use of ocean sound as a central ecological trait in a healthy ocean.

Volumetric analysis and morphological assessment of the ascending olfactory pathway in an elasmobranch and a teleost using diceCT.

The size (volume or mass) of the olfactory bulbs in relation to the whole brain has been used as a neuroanatomical proxy for olfactory capability in a range of vertebrates, including fishes. Here, we use diffusible iodine-based contrast-enhanced computed tomography (diceCT) to test the value of this novel bioimaging technique for generating accurate measurements of the relative volume of the main olfactory brain areas (olfactory bulbs, peduncles, and telencephalon) and to describe the morphological organisation of the ascending olfactory pathway in model fish species from two taxa, the brownbanded bamboo shark Chiloscyllium punctatum and the common goldfish Carassius auratus. We also describe the arrangement of primary projections to the olfactory bulb and secondary projections to the telencephalon in both species. Our results identified substantially larger olfactory bulbs and telencephalon in C. punctatum compared to C. auratus (comprising approximately 5.2% vs. 1.8%, and 51.8% vs. 11.8% of the total brain volume, respectively), reflecting differences between taxa, but also possibly in the role of olfaction in the sensory ecology of these species. We identified segregated primary projections to the bulbs, associated with a compartmentalised olfactory bulb in C. punctatum, which supports previous findings in elasmobranch fishes. DiceCT imaging has been crucial for visualising differences in the morphological organisation of the olfactory system of both model species. We consider comparative neuroanatomical studies between representative species of both elasmobranch and teleost fish groups are fundamental to further our understanding of the evolution of the olfactory system in early vertebrates and the neural basis of olfactory abilities.

Assessing and mitigating impacts of motorboat noise on nesting damselfish.

Motorboats are a pervasive, growing source of anthropogenic noise in marine environments, with known impacts on fish physiology and behaviour. However, empirical evidence for the disruption of parental care remains scarce and stems predominantly from playback studies. Additionally, there is a paucity of experimental studies examining noise-mitigation strategies. We conducted two field experiments to investigate the effects of noise from real motorboats on the parental-care behaviours of a common coral-reef fish, the Ambon damselfish Pomacentrus amboinensis, which exhibits male-only egg care. When exposed to motorboat noise, we found that males exhibited vigilance behaviour 34% more often and spent 17% more time remaining vigilant, compared to an ambient-sound control. We then investigated nest defence in the presence of an introduced conspecific male intruder, incorporating a third noise treatment of altered motorboat-driving practice that was designed to mitigate noise exposure via speed and distance limitations. The males spent 22% less time interacting with the intruder and 154% more time sheltering during normal motorboat exposure compared to the ambient-sound control, with nest-defence levels in the mitigation treatment equivalent to those in ambient conditions. Our results reveal detrimental impacts of real motorboat noise on some aspects of parental care in fish, and successfully demonstrate the positive effects of an affordable, easily implemented mitigation strategy. We strongly advocate the integration of mitigation strategies into future experiments in this field, and the application of evidence-based policy in our increasingly noisy world.

Underwater hearing in sea snakes (Hydrophiinae): first evidence of auditory evoked potential thresholds.

The viviparous sea snakes (Hydrophiinae) are a secondarily aquatic radiation of more than 60 species that possess many phenotypic adaptations to marine life. However, virtually nothing is known of the role and sensitivity of hearing in sea snakes. This study investigated the hearing sensitivity of the fully marine sea snake Hydrophis stokesii by measuring auditory evoked potential (AEP) audiograms for two individuals. AEPs were recorded from 40 Hz (the lowest frequency tested) up to 600 Hz, with a peak in sensitivity identified at 60 Hz (163.5 dB re. 1 µPa or 123 dB re. 1 µm s-2). Our data suggest that sea snakes are sensitive to low-frequency sounds but have relatively low sensitivity compared with bony fishes and marine turtles. Additional studies are required to understand the role of sound in sea snake life history and further assess these species' vulnerability to anthropogenic noise.

Ultrastructural evidence of a mechanosensory function of scale organs (sensilla) in sea snakes (Hydrophiinae).

The evolution of epidermal scales was a major innovation in lepidosaurs, providing a barrier to dehydration and physical stress, while functioning as a sensitive interface for detecting mechanical stimuli in the environment. In snakes, mechanoreception involves tiny scale organs (sensilla) that are concentrated on the surface of the head. The fully marine sea snakes (Hydrophiinae) are closely related to terrestrial hydrophiine snakes but have substantially more protruding (dome-shaped) scale organs that often cover a larger portion of the scale surface. Various divergent selection pressures in the marine environment could account for this morphological variation relating to detection of mechanical stimuli from direct contact with stimuli and/or indirect contact via water motion (i.e. 'hydrodynamic reception'), or co-option for alternate sensory or non-sensory functions. We addressed these hypotheses using immunohistochemistry, and light and electron microscopy, to describe the cells and nerve connections underlying scale organs in two sea snakes, Aipysurus laevis and Hydrophis stokesii. Our results show ultrastructural features in the cephalic scale organs of both marine species that closely resemble the mechanosensitive Meissner-like corpuscles that underlie terrestrial snake scale organs. We conclude that the scale organs of marine hydrophiines have retained a mechanosensory function, but future studies are needed to examine whether they are sensitive to hydrodynamic stimuli.

The effect of underwater sounds on shark behaviour.

The effect of sound on the behaviour of sharks has not been investigated since the 1970s. Sound is, however, an important sensory stimulus underwater, as it can spread in all directions quickly and propagate further than any other sensory cue. We used a baited underwater camera rig to record the behavioural responses of eight species of sharks (seven reef and coastal shark species and the white shark, Carcharodon carcharias) to the playback of two distinct sound stimuli in the wild: an orca call sequence and an artificially generated sound. When sounds were playing, reef and coastal sharks were less numerous in the area, were responsible for fewer interactions with the baited test rigs, and displayed less 'inquisitive' behaviour, compared to during silent control trials. White sharks spent less time around the baited camera rig when the artificial sound was presented, but showed no significant difference in behaviour in response to orca calls. The use of the presented acoustic stimuli alone is not an effective deterrent for C. carcharias. The behavioural response of reef sharks to sound raises concern about the effects of anthropogenic noise on these taxa.

Not all electric shark deterrents are made equal: Effects of a commercial electric anklet deterrent on white shark behaviour.

Personal shark deterrents offer the potential of a non-lethal solution to protect individuals from negative interactions with sharks, but the claims of effectiveness of most deterrents are based on theory rather than robust testing of the devices themselves. Therefore, there is a clear need for thorough testing of commercially available shark deterrents to provide the public with information on their effectiveness. Using a modified stereo-camera system, we quantified behavioural interactions between Carcharodon carcharias (white sharks) and a baited target in the presence of a commercially available electric anklet shark deterrent, the Electronic Shark Defense System (ESDS). The stereo-camera system enabled accurate assessment of the behavioural responses of C. carcharias when approaching an ESDS. We found that the ESDS had limited meaningful effect on the behaviour of C. carcharias, with no significant reduction in the proportion of sharks interacting with the bait in the presence of the active device. At close proximity (< 15.5 cm), the active ESDS did show a significant reduction in the number of sharks biting the bait, but this was countered by an increase in other, less aggressive, interactions. The ESDS discharged at a frequency of 7.8 Hz every 5.1 s for 2.5 s, followed by an inactive interval of 2.6 s. As a result, many sharks may have encountered the device in its inactive state, resulting in a reduced behavioural response. Consequently, decreasing the inactive interval between pulses may improve the overall effectiveness of the device, but this would not improve the effective deterrent range of the device, which is primarily a factor of the voltage gradient rather than the stimulus frequency. In conclusion, given the very short effective range of the ESDS and its unreliable deterrent effect, combined with the fact that shark-bite incidents are very rare, it is unlikely that the current device would significantly reduce the risk of a negative interaction with C. carcharias.

How Close is too Close? The Effect of a Non-Lethal Electric Shark Deterrent on White Shark Behaviour.

Sharks play a vital role in the health of marine ecosystems, but the potential threat that sharks pose to humans is a reminder of our vulnerability when entering the ocean. Personal shark deterrents are being marketed as the solution to mitigate the threat that sharks pose. However, the effectiveness claims of many personal deterrents are based on our knowledge of shark sensory biology rather than robust testing of the devices themselves, as most have not been subjected to independent scientific studies. Therefore, there is a clear need for thorough testing of commercially available shark deterrents to provide the public with recommendations of their effectiveness. Using a modified stereo-camera system, we quantified behavioural interactions between white sharks (Carcharodon carcharias) and a baited target in the presence of a commercially available, personal electric shark deterrent (Shark Shield Freedom7™). The stereo-camera system enabled an accurate assessment of the behavioural responses of C. carcharias when encountering a non-lethal electric field many times stronger than what they would naturally experience. Upon their first observed encounter, all C. carcharias were repelled at a mean (± std. error) proximity of 131 (± 10.3) cm, which corresponded to a mean voltage gradient of 9.7 (± 0.9) V/m. With each subsequent encounter, their proximity decreased by an average of 11.6 cm, which corresponded to an increase in tolerance to the electric field by an average of 2.6 (± 0.5) V/m per encounter. Despite the increase in tolerance, sharks continued to be deterred from interacting for the duration of each trial when in the presence of an active Shark Shield™. Furthermore, the findings provide no support to the theory that electric deterrents attract sharks. The results of this study provide quantitative evidence of the effectiveness of a non-lethal electric shark deterrent, its influence on the behaviour of C. carcharias, and an accurate method for testing other shark deterrent technologies.

Strategic reduction of help before dispersal in a cooperative breeder.

In cooperative breeders, sexually mature subordinates can either queue for chances to inherit the breeding position in their natal group, or disperse to reproduce independently. The choice of one or the other option may be flexible, as when individuals respond to attractive dispersal options, or they may reflect fixed life-history trajectories. Here, we show in a permanently marked, natural population of the cooperatively breeding cichlid fish Neolamprologus pulcher that subordinate helpers reduce investment in territory defence shortly before dispersing. Such reduction of effort is not shown by subordinates who stay and inherit the breeding position. This difference suggests that subordinates ready to leave reduce their investment in the natal territory strategically in favour of future life-history perspectives. It seems to be part of a conditional choice of the dispersal tactic, as this reduction in effort appears only shortly before dispersal, whereas philopatric and dispersing helpers do not differ in defence effort earlier in life. Hence, cooperative territory defence is state-dependent and plastic rather than a consistent part of a fixed life-history trajectory.

Maternal effect on female caste determination in a social insect.

Caste differentiation and division of labor are the hallmarks of social insect colonies [1, 2]. The current dogma for female caste differentiation is that female eggs are totipotent, with morphological and physiological differences between queens and workers stemming from a developmental switch during the larval stage controlled by nutritional and other environmental factors (e.g., [3-8]). In this study, we tested whether maternal effects influence caste differentiation in Pogonomyrmex harvester ants. By conducting crossfostering experiments we identified two key factors in the process of caste determination. New queens were produced only from eggs laid by queens exposed to cold. Moreover, there was a strong age effect, with development into queens occurring only in eggs laid by queens that were at least two years old. Biochemical analyses further revealed that the level of ecdysteroids was significantly lower in eggs developing into queens than workers. By contrast, we found no significant effect of colony size or worker exposure to cold, suggesting that the trigger for caste differentiation may be independent of the quantity and quality of resources provided to larvae. Altogether these data demonstrate that the developmental fate of female brood is strongly influenced by maternal effects in ants of the genus Pogonomyrmex.