Snapshot recordings provide a first description of the acoustic signatures of deeper habitats adjacent to coral reefs of Moorea

Introduction

The existence of coral reefs at depths of more than 150 m in tropical regions has been known for decades (Fricke & Schuhmacher, 1983; Maragos & Jokiel, 1985; Kahng & Maragos, 2006). Recently, the conservation and management of these so-called mesophotic coral ecosystems (MCEs) has been considered a priority, although the reefs themselves remain largely unexplored (Pyle et al., 2016). More generally, deeper zones and habitats close to coral reefs may serve as refuges and be the origin of recruits that contribute to the recovery of reefs located in shallow waters (Bongaerts et al., 2010; Van Oppen et al., 2011). Deeper habitats were, at first, thought to be more protected from temperature increases and coral bleaching events, since the impacts of human and natural perturbations typically diminish with depth and distance from shore (Glynn, 1996; Feingold, 2001; Glynn et al., 2001; Bak, Nieuwland & Meesters, 2005). However, the current degree of global climate change may also have an impact upon deeper habitats (Appeldoorn et al., 2016). Very little is known about MCEs, and the deeper habitats adjacent to coral reefs. Hence, there is a wide range of possible topics to be investigated. As an example, being able to provide an acoustic description of such habitats may appear crucial for extending our current knowledge on marine soundscapes. In particular, it may provide insights into the qualities and characteristics of the deeper habitats associated with coral ecosystems (Staaterman et al., 2014; Bertucci et al., 2015; Nedelec et al., 2015; Bobryk et al., 2016).

A soundscape is defined as the collection of all sounds that are present in a landscape, which vary over space and time (Southworth, 1969; Schafer, 1977; Krause, 1987; Pijanowski et al., 2011). Within soundscapes, sound sources are divided into three main components: the biophony (corresponding to biologically produced sounds), the geophony (the geophysically produced sounds) and the anthropophony (the sounds produced by human activities). The collection of data regarding the nature and qualities of marine soundscapes is growing worldwide (Cato & McCauley, 2002; Chapman & Price, 2011; Bertucci et al., 2016) but despite their potential, investigations of temporal and spatial variations in the soundscapes of coral reefs have mainly been concentrated on comparing neighbouring sites consisting of different habitat types, e.g., mangrove, fringing reef and barrier reef, and they have been restricted to the first 10–20 m of the water column (Piercy et al., 2014; Radford, Stanley & Jeffs, 2014; Bertucci et al., 2015). For instance, Staaterman et al. (2014) described marine soundscapes of Florida reefs in 7 m of water while only the 0–5 m range was recorded in a French Polynesian reef by Nedelec et al. (2015), and in a temperate coastal marine environment by Rossi, Connell & Nagelkerken (2016). Overall, the studies highlighted that different habitat types are characterised by peculiar acoustic features that constitute their acoustic signatures. When assessing the relationship between biodiversity and soundscape features of similar reefs habitats in Virgin Islands and French Polynesia, recordings performed by Kaplan et al. (2015) and Bertucci et al. (2016) were carried out at 18 m and 10 m depth, respectively.

These studies performed in shallow waters demonstrate that acoustical differences between reef habitats are due to variations in the sonic activity of marine organisms, i.e., soniferous fishes, snapping shrimps (Radford, Stanley & Jeffs, 2014) and the geo-morphology of recorded sites. Acoustic cues within habitats close to coral reefs are known to influence the behaviour and orientation of many fish and invertebrate larvae at settlement (Simpson et al., 2004; Vermeij et al., 2010; Nedelec et al., 2015; Parmentier et al., 2015). Describing soundscapes from deeper habitats could further highlight the importance of acoustic cues in the distribution of marine organisms, and the attractiveness of deeper habitats associated with reefs. Many coral reef-associated fish species have highly specialized habitat requirements. Some species are typically found in sandy patches while some other will use different types of coral as shelters, which will lead to differing species assemblages (Bacchet, Zysman & Lefèvre, 2006). Vocal species from these assemblages should create differential acoustic signatures in the frequency range in which they produce sounds. From this perspective, the objective of the present study was to investigate the variations of sound pressure levels in the low frequency range between underexplored habitats adjacent to coral reefs on the north coast of Moorea Island, French Polynesia (17°30′S, 149°5′W) and thereby provide a first insight into the acoustic features of these biotopes.

Material & Methods

Results

Spectral signatures of deeper habitats are mainly characterized by lower sound intensities

For each transect, BR locations presented spectra with significantly higher average sound pressure levels, followed by SP, RS and DO. Average sound pressure levels decreased from BR towards the most distant and deepest habitat, i.e., DO (Kruskal–Wallis, χ² = 19.24 − 30.62, df = 3, all P-values <10⁻³; Tukey’s post-hoc tests for pairwise comparisons) (Fig. 2). For transect 1, BR showed significantly higher average sound pressure levels than the 3 other habitats for all frequencies above 100 Hz. SP showed significantly higher average sound pressure levels than RS and DO from 150 Hz to 2,500 Hz (only a narrow 2,200 Hz–2,300 Hz range did not differ significantly between SP and RS). RS and DO spectra were not significantly different for any frequencies but a narrow frequency band from 1,250 Hz to 1,400 Hz (Two-way ANOVA, F_3,116 = 2.00 − 2.70; P < 0.05) (Fig. 3A). For transect 2, BR and SP differed significantly only from 400 Hz to 1,500 Hz. As for transect 1, RS and DO showed significantly lower intensities than BR for most frequencies, and were significantly lower in their intensities than SP for frequencies below 2,000 Hz. In contrast to transect 1, RS showed significantly higher average sound pressure levels than DO for frequencies below 750 Hz, between 1,400 Hz and 1,500 Hz, and from 2,000 Hz to 2,300 Hz (Two-way ANOVA, F_3,116 = 2.50 ; P < 0.05) (Fig. 3B). For transect 3, all spectra but RS and DO were significantly different for all frequencies from 400 Hz to 2,000 Hz with decreasing intensities from BR to DO. BR showed significantly higher intensities at lower frequencies too and significantly higher intensities than RS and DO above 2,000 Hz. RS and DO did not differ significantly in their intensities except for a very narrow 1,100 Hz –1,200 Hz band caused by the absence of a peak present in the other spectra (Two-way ANOVA, F_3,116 = 2.30 ; P < 0.05) (Fig. 3C).

Similar habitats show differences in their spectral signatures

At the habitat type level, BRs and RSs showed the greatest difference in power spectra between the three transects. For BR, transect 1 showed significantly higher intensities for all frequencies of the spectrum compared to transect 2. The spectrum of BR of transect 2 was characterised by two intensity peaks around 600 Hz and 1,200 Hz. The spectra of transects 1 and 3 differed significantly for frequencies above 1,250 Hz. BR spectra of transects 2 and 3 differed significantly only for a narrow frequency range between 1,250 Hz and 1,500 Hz (Two-way ANOVA, F_2,116 = 2.80 ; P < 0.05) (Fig. 4). For RS, transect 1 showed the significantly highest intensities for most frequencies above 500 Hz while transects 2 and 3 were similar (Two-way ANOVA, F_2,116 = 2.45 ; P < 0.05) (Fig. 4). Spectra of SP and DO showed little variation in their intensities between the three transects. DO of transect 1 showed higher intensities below 400 Hz than DO of transect 2; and DO of transect 2 and 3 differed for higher frequencies between 1,600 Hz and 2,300 Hz (Two-way ANOVA, F_2,116 = 2.35 − 3.00; P < 0.05) (Fig. 4).

The BR of transect 1 displayed the highest average sound pressure level (Kruskal–Wallis, χ² = 11.24, df = 2, P = 0.004, Tukey’s post-hoc tests for pairwise comparisons, all P-values < 0.05) (Fig. 5). No difference was observed between BRs of transect 2 and 3. The power spectra of SPs showed an inverted pattern with SP of transect 1 showing the lowest average sound pressure level (Kruskal–Wallis, χ² = 10.27, df = 2, P = 0.006, Tukey’s post-hoc tests for pairwise comparisons, all P-values < 0.05) (Fig. 5). No difference was observed between SPs of transect 2 and 3. RS and DO showed the significantly lowest sound pressure level for all transects (Kruskal-Wallis, χ² = 19.24 − 30.62, df = 3, all P-values < 10⁻³; Tukey’s post-hoc tests for pairwise comparisons) with all values below 92 dB re: 1 µPa. RS of transect 2 showed significantly lower average sound pressure level (Kruskal-Wallis, χ² = 9.08, df = 2, P = 0.010, Tukey’s post-hoc tests for pairwise comparisons, all P-values < 0.05). The DO of transect 2 showed a significantly higher average sound pressure level of 95 dB re: 1µPa (Kruskal-Wallis, χ² = 13.14, df = 2, P = 0.001, Tukey’s post-hoc tests for pairwise comparisons, all P-values < 0.05) (Fig. 5).

Discussion

Recent studies on coral reefs have highlighted the positive relationships between sound signatures and coral cover, density of fishes or increased number of biotic sound sources in shallow waters (Kaplan et al., 2015; Nedelec et al., 2015; Bertucci et al., 2016). In this study, comparison of the spectra of four types of habitats adjacent to coral reefs, characterized by different topographies and substrates, by increasing depths and distances from the reef, revealed different spectral profiles most probably related to their different physical and biological properties.

Recordings made at the barrier reef presented higher sound pressure levels in the low frequency range despite the fact that low frequencies transmit poorly in shallow waters (Rogers & Cox, 1988). The higher level of the biophony would suggest this habitat type is occupied by more vocal organisms than the three others. We cannot exclude, however, the possibilty that low frequencies are related to a greater contribution of the geophony at the barrier reefs, with sounds produced by crashing waves or by moving substrate (sand) leading to increased sound pressure levels. The short distance between the sea surface and the bottom can also produce more reverberation in shallow waters than in deeper waters and increase sound levels at higher frequencies. Hence, lower sound levels in deeper habitats do not necessarily mean that mesophotic reefs would be less acoustically rich than barrier reefs. A description of potential vocal species present in these habitats together with the description of their physical environments may help to distinguish between the respective contributions from different sources, i.e., biophony and geophony.

Recorded sound pressure levels in deeper habitats highlight that sounds do not result from the sole propagation and degradation of sounds produced at the level of the noisy barrier reef, as predicted by propagation models (Mann et al., 2007) (Table 2). Moreover, sound levels of sandy plains of transects 2 and 3 showed higher average sound levels than their counterpart of transect 1 despite being more distant from their respective barrier reefs. This clearly supports that barrier reef is not the only sound source and that deeper habitats possess their own sound sources. The weak variations between the sandy plain spectra may result from their topography and physical characteristics with large patchy rocky habitats and similar communities between sites. At reef slopes, more distinct signatures appear again with reef slope of transect 3 being as noisy as reef slope of transect 1 despite being located further away from the barrier. Finally, while the spectra of drop-offs of transects 1 and 3 show no significant variations with their respective reef slopes, drop-off at transect 2 was characterized by a higher sound pressure level compared to its reef slope, especially at the low frequencies. So, the decrease of sound intensities along transects appears to be variable and the spectral profiles of the different habitats show significantly increased intensities despite their distance to the barrier reef. These observations would reinforce the idea that the barrier reef is not the single sound source responsible of observed spectra and that additional sources such as soniferous species—that are not present at the level of the barrier or may differ in abundance at deeper habitats—may actively play a role in the sonic signature of deeper environments. In particular, as the transitions between the reef slopes and the reef drop-offs are very short for all transects, the observed differences (especially for transect 2) between spectra and the potential link with differential biological activity deserve to be investigated. Indeed, while the reef slope is a zone of sedimentary accumulation with a low species richness, the reef drop-off houses numerous fish species. This might explain the increased intensities between these 2 types of habitats.

Overall, as in shallow waters, differences in spectral patterns seem to exist in deeper habitats and may therefore reflect different characteristics of the habitats, i.e., physical and/or biological. Acoustic cues produced by deeper habitats may therefore also be used in the orientation of marine larvae and may come into play earlier in the recruitment of coral reefs organisms. However, the short period of time sampled in this study remains insufficient to reliably characterize the different habitats and only provides initial information on the different acoustic signatures of deeper habitats. Fish vocal activity can change drastically at dusk or dawn and be more sustained at night with specific species vocalizing in specific time windows (Pieretti et al., 2017). Monitoring for longer time periods might highlight further differences between habitats at the diel scale. Moreover, sound production in fishes is often linked to social activities, such as courtship interactions and spawning events that will vary on a longer, seasonal scale. Long term recordings of deeper environments would then be necessary to capture the complete picture and identify acoustic differences (Pieretti et al., 2017).

Conclusion

We still know very little about the acoustic ecology of deeper habitats adjacent to coral reefs. It has been assumed that deeper environments were less likely to be impacted by anthropogenic activities or by global change, and therefore may provide refuge areas for shallow reef species (Bongaerts et al., 2010). This hypothesis has gained a growing interest in the scientific community, but has been only tested at few locations for few species. In the future, the opportunity to have proxies of the ecological state of these refuge areas by means of soundscape analysis and linking their acoustic characteristics to their refuge potential may help to better judge the impact of global change and the influence of these adjacent ecosystems on coral reefs. Several studies have demonstrated that barrier reef sound attracts fish and crustacean larvae during settlement onto the reef (Barth et al., 2015). The present study represents a first step towards the acoustic investigation of deeper environments and suggests that deeper habitats could also play a role in the orientation of larval marine organisms.

Research in practically unexplored depths will undoubtedly bring new knowledge and tools that will be extremely valuable for the creation of Marine Protected Areas (MPAs), watershed management plans and the development of conservation plans for coral reefs as a whole, from shallow to deep water habitats.