Behavioural response thresholds in New Zealand crab megalopae to ambient underwater sound

A small number of studies have demonstrated that settlement stage decapod crustaceans are able to detect and exhibit swimming, settlement and metamorphosis responses to ambient underwater sound emanating from coastal reefs. However, the intensity of the acoustic cue required to initiate the settlement and metamorphosis response, and therefore the potential range over which this acoustic cue may operate, is not known. The current study determined the behavioural response thresholds of four species of New Zealand brachyuran crab megalopae by exposing them to different intensity levels of broadcast reef sound recorded from their preferred settlement habitat and from an unfavourable settlement habitat. Megalopae of the rocky-reef crab, Leptograpsus variegatus, exhibited the lowest behavioural response threshold (highest sensitivity), with a significant reduction in time to metamorphosis (TTM) when exposed to underwater reef sound with an intensity of 90 dB re 1 μPa and greater (100, 126 and 135 dB re 1 μPa). Megalopae of the mud crab, Austrohelice crassa, which settle in soft sediment habitats, exhibited no response to any of the underwater reef sound levels. All reef associated species exposed to sound levels from an unfavourable settlement habitat showed no significant change in TTM, even at intensities that were similar to their preferred reef sound for which reductions in TTM were observed. These results indicated that megalopae were able to discern and respond selectively to habitat-specific acoustic cues. The settlement and metamorphosis behavioural response thresholds to levels of underwater reef sound determined in the current study of four species of crabs, enables preliminary estimation of the spatial range at which an acoustic settlement cue may be operating, from 5 m to 40 km depending on the species. Overall, these results indicate that underwater sound is likely to play a major role in influencing the spatial patterns of settlement of coastal crab species.     

Temporal and Spatial Comparisons of Underwater Sound Signatures of Different Reef Habitats in Moorea Island,French Polynesia

As environmental sounds are used by larval fish and crustaceans to locate and orientate towards habitat during settlement, variations in the acoustic signature produced by habitats could provide valuable information about habitat quality, helping larvae to differentiate between potential settlement sites. However, very little is known about how acoustic signatures differ between proximate habitats. This study described within- and between-site differences in the sound spectra of five contiguous habitats at Moorea Island, French Polynesia: the inner reef crest, the barrier reef, the fringing reef, a pass and a coastal mangrove forest. Habitats with coral (inner, barrier and fringing reefs) were characterized by a similar sound spectrum with average intensities ranging from 70 to 78 dB re 1μPa.Hz^-1. The mangrove forest had a lower sound intensity of 70 dB re 1μPa.Hz^-1 while the pass was characterized by a higher sound level with an average intensity of 91 dB re 1μPa.Hz^-1. Habitats showed significantly different intensities for most frequencies, and a decreasing intensity gradient was observed from the reef to the shore. While habitats close to the shore showed no significant diel variation in sound intensities, sound levels increased at the pass during the night and barrier reef during the day. These two habitats also appeared to be louder in the North than in the West. These findings suggest that daily variations in sound intensity and across-reef sound gradients could be a valuable source of information for settling larvae. They also provide further evidence that closely related habitats, separated by less than 1 km, can differ significantly in their spectral composition and that these signatures might be typical and conserved along the coast of Moorea.     

Oyster Larvae Settle in Response to Habitat-Associated Underwater Sounds

Following a planktonic dispersal period of days to months, the larvae of benthic marine organisms must locate suitable seafloor habitat in which to settle and metamorphose. For animals that are sessile or sedentary as adults, settlement onto substrates that are adequate for survival and reproduction is particularly critical, yet represents a challenge since patchily distributed settlement sites may be difficult to find along a coast or within an estuary. Recent studies have demonstrated that the underwater soundscape, the distinct sounds that emanate from habitats and contain information about their biological and physical characteristics, may serve as broad-scale environmental cue for marine larvae to find satisfactory settlement sites. Here, we contrast the acoustic characteristics of oyster reef and off-reef soft bottoms, and investigate the effect of habitat-associated estuarine sound on the settlement patterns of an economically and ecologically important reef-building bivalve, the Eastern oyster (Crassostrea virginica). Subtidal oyster reefs in coastal North Carolina, USA show distinct acoustic signatures compared to adjacent off-reef soft bottom habitats, characterized by consistently higher levels of sound in the 1.5–20 kHz range. Manipulative laboratory playback experiments found increased settlement in larval oyster cultures exposed to oyster reef sound compared to unstructured soft bottom sound or no sound treatments. In field experiments, ambient reef sound produced higher levels of oyster settlement in larval cultures than did off-reef sound treatments. The results suggest that oyster larvae have the ability to respond to sounds indicative of optimal settlement sites, and this is the first evidence that habitat-related differences in estuarine sounds influence the settlement of a mollusk. Habitat-specific sound characteristics may represent an important settlement and habitat selection cue for estuarine invertebrates and could play a role in driving settlement and recruitment patterns in marine communities.     

Directional orientation of pomacentrid larvae to ambient reef sound

The mechanisms by which reef fish larvae locate settlement habitat at the end of their pelagic phase are unclear. We used an in situ binary choice chamber and an artificial source of reef sound to determine whether pomacentrid larvae can use ambient sound to locate reefs. Larvae were caught in light traps and then placed in a submerged binary choice chamber with an artificial source of reef sound ~80 m from one end of the chamber. At night, larvae moved towards the sound source; during the day, larvae showed no preference. These results suggest that pomacentrid larvae can detect reef sound and are capable of directional hearing. While other studies have shown that reef fish larvae respond to reef sound, and that the adults of some species can localize underwater sound sources, the localization of underwater sound by fish larvae has not been demonstrated previously.Communicated by Ecological Editor P.F. Sale     

Sources and Levels of Ambient Ocean Sound near the Antarctic Peninsula

Arrays of hydrophones were deployed within the Bransfield Strait and Scotia Sea (Antarctic Peninsula region) from 2005 to 2009 to record ambient ocean sound at frequencies of up to 125 and 500 Hz. Icequakes, which are broadband, short duration signals derived from fracturing of large free-floating icebergs, are a prominent feature of the ocean soundscape. Icequake activity peaks during austral summer and is minimum during winter, likely following freeze-thaw cycles. Iceberg grounding and rapid disintegration also releases significant acoustic energy, equivalent to large-scale geophysical events. Overall ambient sound levels can be as much as ~10–20 dB higher in the open, deep ocean of the Scotia Sea compared to the relatively shallow Bransfield Strait. Noise levels become lowest during the austral winter, as sea-ice cover suppresses wind and wave noise. Ambient noise levels are highest during austral spring and summer, as surface noise, ice cracking and biological activity intensifies. Vocalizations of blue (Balaenoptera musculus) and fin (B. physalus) whales also dominate the long-term spectra records in the 15–28 and 89 Hz bands. Blue whale call energy is a maximum during austral summer-fall in the Drake Passage and Bransfield Strait when ambient noise levels are a maximum and sea-ice cover is a minimum. Fin whale vocalizations were also most common during austral summer-early fall months in both the Bransfield Strait and Scotia Sea. The hydrophone data overall do not show sustained anthropogenic sources (ships and airguns), likely due to low coastal traffic and the typically rough weather and sea conditions of the Southern Ocean.     

Parasites of coral reef fish larvae: its role in the pelagic larval stage

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, detrimental consequences for the hosts. However, little is known about the parasites that larval fish have upon settlement, and the factors that affect the levels of parasitism. At settlement, coral reef fishes vary greatly in size and age (pelagic larval duration), which may influence the degree of parasitism. We identified and quantified the parasites of pre-settlement larvae from 44 species of coral reef fishes from the Great Barrier Reef and explored their relationship with host size and age at settlement, and phylogeny. Overall, less than 50% of the larval fishes were infected with parasites, and over 99% of these were endoparasites. A Bayesian phylogenetic regression was used to analyse host-parasite (presence and intensity) associations. The analysis showed parasite presence was not significantly related to fish size, and parasite intensity was not significantly related to fish age. A phylogenetic signal was detected for both parasite presence and intensity, indicating that, overall, closely related fish species were likely to have more similar susceptibility to parasites and similar levels of parasitism when compared to more distantly related species. The low prevalence of infection with any parasite type and the striking rarity of ectoparasites is consistent with the ‘parasite avoidance hypothesis’, which proposes that the pelagic phase of coral reef fishes results in reduced levels of parasitism.

     

Soundscapes from a Tropical Eastern Pacific reef and a Caribbean Sea reef

Underwater soundscapes vary due to the abiotic and biological components of the habitat. We quantitatively characterized the acoustic environments of two coral reef habitats, one in the Tropical Eastern Pacific (Panama) and one in the Caribbean (Florida Keys), over 2-day recording durations in July 2011. We examined the frequency distribution, temporal variability, and biological patterns of sound production and found clear differences. The Pacific reef exhibited clear biological patterns and high temporal variability, such as the onset of snapping shrimp noise at night, as well as a 400-Hz daytime band likely produced by damselfish. In contrast, the Caribbean reef had high sound levels in the lowest frequencies, but lacked clear temporal patterns. We suggest that acoustic measures are an important element to include in reef monitoring programs, as the acoustic environment plays an important role in the ecology of reef organisms at multiple life-history stages.     

Early life history and settlement of the slender filefish, <Emphasis Type="Italic">Monacanthus tuckeri</Emphasis> (Monacanthidae), at Calabash Caye,Turneffe Atoll,Belize

Synopsis We examined early life history traits and patterns of settlement of the slender filefish, Monacanthus tuckeri, at Calabash Caye, Turneffe Atoll, Belize. A settlement peak was evident at the new moon, and no settlement occurred at the full moon. However, settlement rates at the quarter moons could not be estimated due to sampling gaps. Many reef fishes show new moon settlement peaks, so M. tuckeri shares some characteristics with the primarily perciform species on coral reefs. Pelagic larval duration was long (mean = 42 days) and variable, suggesting that dispersal patterns might be diverse. Size at settlement was large (mean = 32 mm total length) and also variable. Larval duration and size at settlement were outside of the average values exhibited by reef fishes, but are not beyond the extreme end of the range, and might be explained by association with pelagic debris prior to settlement. There were no differences in overall settlement rates on reef and seagrass habitats, and fish settling to either habitat did not differ in larval duration, size at settlement, or larval growth rate. This suggests that settlement to alternative habitats may be random, or driven by availability of suitable microhabitat, rather than habitat quality or individual traits.     

Variability in spatial and temporal occurrence of presettlement and settlement‐stage fishes associated with shallow reefs

Presettlement and settlement‐stage fishes were studied in a large, log‐spiral bay in temperate South Africa. The aim was to describe the assemblage composition, density and distribution associated with four types of habitats common to the bay: high profile reef, low profile reef, reef‐associated sand and open sand spatially separated from reef. Samples were collected with both a plankton ring net and a light trap at each habitat type as part of a mixed‐method approach. A total of 4084 presettlement and settlement‐stage fishes belonging to 31 teleost families and 84 species were captured. Reef‐associated sand and open sand habitats yielded higher species richness and diversity than the high and low‐profile reef habitats. Engraulidae, Gobiidae, Clupeidae and Cynoglossidae were the dominant fish families captured with the ring net, while Engraulidae, Clupeidae, Carangidae and Clinidae were captured with the light trap. A temporal difference in the abundance of presettlement fishes occurred between the sampling periods with highest values recorded during the summer settlement period. Habitat type together with associated physico‐chemical variables played a pivotal role in determining presettlement fish species composition, density and distribution across habitat types.     

Temporal scales of variation in settlement and recruitment of the mussel Perna perna (Linnaeus, 1758)

Population dynamics of many intertidal organisms are strongly affected by the abundance and distribution of larvae arriving on the shore. In particular, not only absolute numbers of settlers but also the degree of synchronisation of settlement can have a strong influence on whether density-dependent or density-independent processes shape adult shape populations. Temporal variation in rates of settlement and recruitment of the mussel Perna perna on the south coast of South Africa was investigated using a nested spatial design at different temporal scales. Variability in settlement at spring tides was examined at two temporal scales: lunar (to investigate the effect of state of the moon on settlement) and tidal (to investigate the influence of state of the tide on mussel settlement). Recruitment over neap tides was examined at one temporal scale, fortnight (to investigate the effect of date on mussel recruitment).Strong temporal variation was evident for both settlement and recruitment, but not at all time scales. Distinct peaks of settler/recruit abundance were observed during the lunar and neap tide studies. Recruitment intensity differed over the course of the year, and pulsing of recruitment was generally synchronised among locations. However, the strength of pulsing differed dramatically among locations, giving a significant interaction between fortnight and location. The finest temporal scale, investigated in the tidal study, did not reveal a significant effect of the state of the tide on settlement. The state of the moon (new or full) was not significant as a main factor (p = 0.052), although generally more settlers arrived on the shore during new moon. Phase of the moon appeared to have an effect on settler abundances, but only when and where densities were high.     

Effects of moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus

Influences of light-dark (LD) cycle and moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus, a lunar synchronized spawner, were determined by time-resolved fluoroimmunoassay (TR-FIA). When the fish were exposed to a natural LD (12:12) cycle, plasma melatonin levels exhibited a clear daily rhythm, with higher levels at midnight and lower levels during the day. These rhythms were not evident under either constant light (LL) or constant dark (DD) conditions. Plasma melatonin levels under LL condition were low and high under DD condition. These results indicate that plasma melatonin rhythms are driven by LD cycle in this species. When the fish were exposed to the 4 lunar phases, plasma melatonin levels around the new moon were significantly higher than during the first quarter moon and the full moon. Exposure to experimental new moon and full moon conditions caused significant increases and decreases of plasma melatonin levels, respectively. The synchronous rhythmicity of melatonin levels in the plasma support the hypothesis that the seagrass rabbitfish perceives moonlight intensity and responds with secretion of melatonin into the bloodstream.     

Sounds of shallow water fishes pitch within the quiet window of the habitat ambient noise

The habitat ambient noise may exert an important selective pressure on frequencies used in acoustic communication by animals. A previous study demonstrated the presence of a match between the low-frequency quiet region of the stream ambient noise (termed ‘quiet window’) and the main frequencies used for sound production and hearing by two stream gobies (Padogobius bonelli, Gobius nigricans). The present study examines the spectral features of ambient noise in very shallow freshwater, brackish and marine habitats and correlates them to the range of dominant frequencies of sounds used by nine species of Mediterranean gobies reproducing in these environments. Ambient noise spectra of these habitats featured a low-frequency quiet window centered at 100 Hz (stream, sandy/rocky sea shore), or at 200 Hz (spring, brackish lagoon). The analysis of the ambient noise/sound spectrum relationships showed the sound frequencies matched the frequency band of the quiet window in the ambient noise typical of their own habitat. Analogous ambient noise/sound frequency relationships were observed in other shallow-water teleosts living in similar underwater environments. Conclusions may be relevant to the understanding of evolution of fish acoustic communication and hearing.     

Urea is a dynamic pool of bioavailable nitrogen in coral reefs

Urea may be an important source of nitrogen in low nutrient coral reef environments because corals and other organisms can assimilate it easily and it is found throughout ocean waters. We measured the distribution and concentrations of urea in seagrass beds, areas of schooling fish, coral formations and bottom sediments in the Upper Florida Keys Reef Tract. The flux of urea from bottom sediments was also measured. Ambient concentrations of urea in the offshore reefs were similar to the concentrations of nitrate and ammonium. Seagrass beds, areas of schooling fish and coral formations had elevated concentrations of urea that were up to eight times higher than nitrate in the system. Numerous ephemeral hotspots of urea that were 8–20 times the ambient urea concentration existed in seagrass beds, areas of schooling fish, and above sediments. Coastal areas and inland canals had high urea concentrations where urban runoff and septic effluents were prevalent, but there was no anthropogenic influence in the offshore habitats. Urea concentrations above bottom sediments were not different from ambient concentrations and benthic flux chamber incubations showed biological activity in carbonaceous sediments but no net urea production. The decrease in urea concentrations from coasts and inland waterways to a consistent ambient concentration in the offshore reef system and ephemeral hotspots of high urea concentration suggest that urea is a dynamic pool of bioavailable nitrogen in the reefs of the Upper Florida Keys.     

Spatiotemporal distribution of nocturnal coral reef fish juveniles in Moorea Island,French Polynesia

This study aimed to investigate the spatial structure of nocturnal fish communities at settlement on coral reefs in Moorea Island lagoon, French Polynesia; and the temporal consistency of habitat selection between winter (April to June 2001) and summer (November 2001). The Moorea lagoon was divided into 12 habitat zones (i.e., coral reef zones), which were distinct in terms of depth, wave exposure, and substratum composition. Nocturnal visual censuses among the 12 habitats found that the recently settled juveniles of 25 species recorded were dispatched among three communities spatially distributed according to the distance from the reef crest (reef crest, barrier reef, and fringing reef communities). This spatial communities structure of nocturnal juveniles was consistent in both winter and summer and would be explained primarily by a current gradient in Moorea lagoon (current speed was high near the reef crest and decreased towards the beach) and by the topographic characteristics of reef zones. Among the 25 species, 13 were recorded in both winter and summer. A comparison of the spatial distribution between summer and winter for 13 species that occurred during both seasons found that only 4 differed between the two seasons. For these species, habitat selection would be organized primarily by some stochastic processes such as inter- and intraspecific competition, predation, and food availability. Overall, the present study allowed us to highlight that most nocturnal coral reef fish juveniles at Moorea Island exhibited striking patterns in their distribution and current and topographic characteristics of reef zones might exert considerable influence on the distribution of fishes.     

Modelling larval dispersal and behaviour of coral reef fishes

Coral reef fish spend their first few weeks developing in the open ocean, where eggs and larvae appear merciless to tides and currents, before attempting to leave the pelagic zone and settle on a suitable reef. This pelagic dispersal phase is the process that determines population connectivity and allows replenishment of harvested populations across multiple coral reef habitats. Until recently this pelagic larval dispersal phase has been poorly understood and has often been referred to as the ‘black-box’ in the life-history of coral reef fishes. In this perspective article we highlight three areas where mathematical and computational approaches have been used to aid our understanding of this important ecological process. We discuss models that provide insights into the evolution of the pelagic larval phase in coral reef fish, an unresolved question which lends itself well to a modelling approach due to the difficulty in obtaining empirical data on this life history strategy. We describe how studies of fish hearing and physical sound propagation models can be used to predict the detection distance of reefs for settling larval fish, and the potential impact of anthropogenic noise. We explain how random walk models can be used to explore individual- and group-level behaviour in larval fish during the dispersal and settlement stage of their life-history. Finally, we discuss the mutual benefits that mathematical and computational approaches have brought to and gained from the field of larval behaviour and dispersal of reef fishes.     

Identifying migratory contingents of fish by combining otolith Sr:Ca with temporal collections of ambient Sr:Ca concentrations

Ambient strontium:calcium (Sr:Ca) concentrations were determined at the temporal scales of months, weeks and days, in summer and winter at two estuarine sites, and experimentally derived correlations between ambient and otolith Sr:Ca were used to estimate the otolith Sr:Ca concentrations of 'resident' black bream Acanthopagrus butcheri . Wild black bream were collected in summer and winter at the end of the temporal water sampling, and their otolith Sr:Ca concentrations were examined. Wild fish were classified as 'resident' if their otolith Sr:Ca matched the predicted concentrations of resident fish, and 'migrant' if this did not occur. In winter, all fish were classified as resident. In summer, all fish were classified as migrants, with fish spending an average of only 16·8% (estuary 1) and 61·1% (estuary 2) of their time at each estuarine location.     

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.     

White Noise Masks Some Temporal Parameters of the Auditory Localization of Radially Moving Targets

The temporal parameters of the perception of radially moving sound sources partly masked with broadband internalized noise at an intensity of 40, 46, or 52 dB above the hearing threshold have been studied. The threshold of sound duration necessary for identifying the direction of movement of the sound source (75% correct answers) increases from 135 ms in silence to 285 ms at all intensities of continuous noise studied. The minimum duration of the stimulus beginning with which a subsequent increase in duration does not increase the number of correct responses is the same (385 ms) under all conditions of stimulus presentation. Broadband noise of any intensity increases the time of response to stimuli in the range of durations studied. At a noise of 52 dB, which is close to the threshold of full masking, the reaction time is not increased significantly compared to its estimation at a noise of 46 dB. The minimum duration of the stimulus has proved to be the stablest temporal parameter of the perception of movement of a sound source. Changes in the temporal parameters of sound perception at noise levels close to the threshold of full masking are discussed.     

Intermittent Noise Induces Physiological Stress in a Coastal Marine Fish

Anthropogenic noise in the ocean has increased substantially in recent decades, and motorized vessels produce what is likely the most common form of underwater noise pollution. Noise has the potential to induce physiological stress in marine fishes, which may have negative ecological consequences. In this study, physiological effects of increased noise (playback of boat noise recorded in the field) on a coastal marine fish (the giant kelpfish, Heterostichus rostratus) were investigated by measuring the stress responses (cortisol concentration) of fish to increased noise of various temporal dynamics and noise levels. Giant kelpfish exhibited acute stress responses when exposed to intermittent noise, but not to continuous noise or control conditions (playback of recorded natural ambient sound). These results suggest that variability in the acoustic environment may be more important than the period of noise exposure for inducing stress in a marine fish, and provide information regarding noise levels at which physiological responses occur.     

Daytime noise predicts nocturnal singing in urban robins

Ambient noise interferes with the propagation of acoustic signals through the environment from sender to receiver. Over the past few centuries, urbanization and the development of busy transport networks have led to dramatic increases in the levels of ambient noise with which animal acoustic communications must compete. Here we show that urban European robins Erithacus rubecula, highly territorial birds reliant on vocal communication, reduce acoustic interference by singing during the night in areas that are noisy during the day. The effect of ambient light pollution, to which nocturnal singing in urban birds is frequently attributed, is much weaker than that of daytime noise.