Stephen D. Simpson

Sound as an Orientation Cue for the Pelagic Larvae of Reef Fishes and Decapod Crustaceans

The pelagic life history phase of reef fishes and decapod crustaceans is complex, and the evolutionary drivers and ecological consequences of this life history strategy remain largely speculative. There is no doubt, however, that this life history phase is very significant in the demographics of reef populations. Here, we initially discuss the ecology and evolution of the pelagic life histories as a context to our review of the role of acoustics in the latter part of the pelagic phase as the larvae transit back onto a reef. Evidence is reviewed showing that larvae are actively involved in this transition. They are capable swimmers and can locate reefs from hundreds of metres if not kilometres away. Evidence also shows that sound is available as an orientation cue, and that fishes and crustaceans hear sound and orient to sound in a manner that is consistent with their use of sound to guide settlement onto reefs. Comparing particle motion sound strengths in the field (8 x 10(-11) m at 5 km from a reef) with the measured behavioural and electrophysiological threshold of fishes of (3 x 10(-11) m and 10 x 10(-11), respectively) provides evidence that sound may be a useful orientation cue at a range of kilometres rather than hundreds of metres. These threshold levels are for adult fishes and we conclude that better data are needed for larval fishes and crustaceans at the time of settlement. Measurements of field strengths in the region of reefs and threshold levels are suitable for showing that sound could be used; however, field experiments are the only effective tool to demonstrate the actual use of underwater sound for orientation purposes. A diverse series of field experiments including light-trap catches enhanced by replayed reef sound, in situ observations of behaviour and sound-enhanced settlement rate on patch reefs collectively provide a compelling case that sound is used as an orientation and settlement cue for these late larval stages.

Ocean acidification erodes crucial auditory behaviour in a marine fish

Ocean acidification is predicted to affect marine ecosystems in many ways, including modification of fish behaviour. Previous studies have identified effects of CO2-enriched conditions on the sensory behaviour of fishes, including the loss of natural responses to odours resulting in ecologically deleterious decisions. Many fishes also rely on hearing for orientation, habitat selection, predator avoidance and communication. We used an auditory choice chamber to study the influence of CO2-enriched conditions on directional responses of juvenile clownfish (Amphiprion percula) to daytime reef noise. Rearing and test conditions were based on Intergovernmental Panel on Climate Change predictions for the twenty-first century: current-day ambient, 600, 700 and 900 µatm pCO2. Juveniles from ambient CO2-conditions significantly avoided the reef noise, as expected, but this behaviour was absent in juveniles from CO2-enriched conditions. This study provides, to our knowledge, the first evidence that ocean acidification affects the auditory response of fishes, with potentially detrimental impacts on early survival.

Coral Larvae Move toward Reef Sounds

Free-swimming larvae of tropical corals go through a critical life-phase when they return from the open ocean to select a suitable settlement substrate. During the planktonic phase of their life cycle, the behaviours of small coral larvae (<1 mm) that influence settlement success are difficult to observe in situ and are therefore largely unknown. Here, we show that coral larvae respond to acoustic cues that may facilitate detection of habitat from large distances and from upcurrent of preferred settlement locations. Using in situ choice chambers, we found that settling coral larvae were attracted to reef sounds, produced mainly by fish and crustaceans, which we broadcast underwater using loudspeakers. Our discovery that coral larvae can detect and respond to sound is the first description of an auditory response in the invertebrate phylum Cnidaria, which includes jellyfish, anemones, and hydroids as well as corals. If, like settlement-stage reef fish and crustaceans, coral larvae use reef noise as a cue for orientation, the alleviation of noise pollution in the marine environment may gain further urgency.

Noise negatively affects foraging and antipredator behaviour in shore crabs

Acoustic noise has the potential to cause stress, to distract and to mask important sounds, and thus to affect behaviour. Human activities have added considerable noise to both terrestrial and aquatic habitats, and there is growing evidence that anthropogenic noise affects communication and movement patterns in a variety of species. However, there has been relatively little work considering the effect on behaviours that are fundamental to survival, and thus have direct fitness consequences. We conducted a series of controlled tank-based experiments to consider how playback of ship noise, the most common source of underwater noise, affects foraging and antipredator behaviour in the shore crab, Carcinus maenas. Ship noise playback was more likely than ambient-noise playback to disrupt feeding, although crabs experiencing the two sound treatments did not differ in their likelihood of, or speed at, finding a food source in the first place. While crabs exposed to ship noise playback were just as likely as ambient-noise controls to detect and respond to a simulated predatory attack, they were slower to retreat to shelter. Ship noise playback also resulted in crabs that had been turned on their backs righting themselves faster than those experiencing ambient-noise playback; remaining immobile may reduce the likelihood of further predatory attention. Our findings therefore suggest that anthropogenic noise has the potential to increase the risks of starvation and predation, and showcases that the behaviour of invertebrates, and not just vertebrates, is susceptible to the impact of this pervasive global pollutant.

A test of the senses: Fish select novel habitats by responding to multiple cues

Habitat-specific cues play an important role in orientation for animals that move through a mosaic of habitats. Environmental cues can be imprinted upon during early life stages to guide later return to adult habitats, yet many species must orient toward suitable habitats without previous experience of the habitat. It is hypothesized that multiple sensory cues may enable animals to differentiate between habitats in a sequential order relevant to the spatial scales over which the different types of information are conveyed, but previous research, especially for marine organisms, has mainly focused on the use of single cues in isolation. In this study, we investigated novel habitat selection through the use of three different sensory modalities (hearing, vision, and olfaction). Our model species, the French grunt, Haemulon flavolineatum, is a mangrove/seagrass-associated reef fish species that makes several habitat transitions during early life. Using several in situ and ex situ experiments, we tested the response of fish toward auditory, olfactory, and visual cues from four different habitats (seagrass beds, mangroves, rubble, and coral reef). We identified receptivity to multiple sensory cues during the same life phase, and found that different cues induced different reactions toward the same habitat. For example, early-juvenile fish only responded to sound from coral reefs and to chemical cues from mangroves/seagrass beds, while visual cues of conspecifics overruled olfactory cues from mangrove/seagrass water. Mapping these preferences to the ecology of ontogenetic movements, our results suggest sequential cue use would indeed aid successful orientation to novel key habitats in early life.

Anthropogenic noise increases fish mortality by predation

Noise-generating human activities affect hearing, communication and movement in terrestrial and aquatic animals, but direct evidence for impacts on survival is rare. We examined effects of motorboat noise on post-settlement survival and physiology of a prey fish species and its performance when exposed to predators. Both playback of motorboat noise and direct disturbance by motorboats elevated metabolic rate in Ambon damselfish (Pomacentrus amboinensis), which when stressed by motorboat noise responded less often and less rapidly to simulated predatory strikes. Prey were captured more readily by their natural predator (dusky dottyback, Pseudochromis fuscus) during exposure to motorboat noise compared with ambient conditions, and more than twice as many prey were consumed by the predator in field experiments when motorboats were passing. Our study suggests that a common source of noise in the marine environment has the potential to impact fish demography, highlighting the need to include anthropogenic noise in management plans.

Size-dependent physiological responses of shore crabs to single and repeated playback of ship noise

Anthropogenic noise has fundamentally changed the acoustics of terrestrial and aquatic environments, and there is growing empirical evidence that even a single noise exposure can affect behaviour in a variety of vertebrate organisms. Here, we use controlled experiments to investigate how the physiology of a marine invertebrate, the shore crab (Carcinus maenas), is affected by both single and repeated exposure to ship-noise playback. Crabs experiencing ship-noise playback consumed more oxygen, indicating a higher metabolic rate and potentially greater stress, than those exposed to ambient-noise playback. The response to single ship-noise playback was size-dependent, with heavier crabs showing a stronger response than lighter individuals. Repeated exposure to ambient-noise playback led to increased oxygen consumption (probably due to handling stress), whereas repeated exposure to ship-noise playback produced no change in physiological response; explanations include the possibility that crabs exhibited a maximal response on first exposure to ship-noise playback, or that they habituated or become tolerant to it. These results highlight that invertebrates, like vertebrates, may also be susceptible to the detrimental impacts of anthropogenic noise and demonstrate the tractability for more detailed investigations into the effects of this pervasive global pollutant.

Acoustic noise reduces foraging success in two sympatric fish species via different mechanisms

Effective foraging behaviour is essential for animals to survive and reproduce, and depends on many intrinsic and environmental factors. There is increasing evidence that man-made (anthropogenic) factors can affect the behaviour of a wide range of taxa. However, few experimental studies have investigated how foraging behaviour is affected by exposure to increased noise levels, an issue of growing global concern. In our laboratory study, we examined how exposure to playback of noise originally recorded from ships, a prevalent source of human-generated underwater noise, affects the feeding behaviour of two sympatric fish species: the three-spined stickleback, Gasterosteus aculeatus, and the European minnow, Phoxinus phoxinus. Both species consumed significantly fewer live Daphnia magna, and showed startle responses significantly more often during playback of additional noise than during control conditions. However, whereas minnows showed a qualitative shift in activity away from foraging behaviour (greater inactivity, more social behaviour) under increased noise conditions, consistent with a classic stress- or fear-related defence cascade, sticklebacks maintained foraging effort but made more mistakes, which may result from an impact of noise on cognition. These findings indicate that additional noise in the environment can lead to reduced food consumption, but that the effects of elevated noise are species specific. It remains to be tested whether these interspecific differences translate into different ultimate impacts, but differential disruptions to foraging may have potential consequences for relative individual fitness and community structure.

Adaptive avoidance of reef noise.

Auditory information is widely used throughout the animal kingdom in both terrestrial and aquatic environments. Some marine species are dependent on reefs for adult survival and reproduction, and are known to use reef noise to guide orientation towards suitable habitat. Many others that forage in food-rich inshore waters would, however, benefit from avoiding the high density of predators resident on reefs, but nothing is known about whether acoustic cues are used in this context. By analysing a sample of nearly 700,000 crustaceans, caught during experimental playbacks in light traps in the Great Barrier Reef lagoon, we demonstrate an auditory capability in a broad suite of previously neglected taxa, and provide the first evidence in any marine organisms that reef noise can act as a deterrent. In contrast to the larvae of species that require reef habitat for future success, which showed an attraction to broadcasted reef noise, taxa with a pelagic or nocturnally emergent lifestyle actively avoided it. Our results suggest that a far greater range of invertebrate taxa than previously thought can respond to acoustic cues, emphasising yet further the potential negative impact of globally increasing levels of underwater anthropogenic noise.

Dispersal without errors: symmetrical ears tune into the right frequency for survival

Vertebrate animals localize sounds by comparing differences in the acoustic signal between the two ears and, accordingly, ear structures such as the otoliths of fishes are expected to develop symmetrically. Sound recently emerged as a leading candidate cue for reef fish larvae navigating from open waters back to the reef. Clearly, the integrity of the auditory organ has a direct bearing on what and how fish larvae hear. Yet, the link between otolith symmetry and effective navigation has never been investigated in fishes. We tested whether otolith asymmetry influenced the ability of returning larvae to detect and successfully recruit to favourable reef habitats. Our results suggest that larvae with asymmetrical otoliths not only encountered greater difficulties in detecting suitable settlement habitats, but may also suffer significantly higher rates of mortality. Further, we found that otolith asymmetries arising early in the embryonic stage were not corrected by any compensational growth mechanism during the larval stage. Because these errors persist and phenotypic selection penalizes asymmetrical individuals, asymmetry is likely to play an important role in shaping wild fish populations.