The biological soundscape of temperate reefs: characterizing natural and artificial reefs in the Dutch Wadden Sea

doi:10.21203/rs.3.rs-4593657/v1

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The biological soundscape of temperate reefs: characterizing natural and artificial reefs in the Dutch Wadden Sea

https://doi.org/10.21203/rs.3.rs-4593657/v1

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Monitoring coastal marine habitats presents many challenges. Often, using multiple approaches to capture different aspects of ecosystems can strengthen the information gained regarding habitat status. The use of passive acoustics to document, describe, and monitor coastal habitats through soundscapes presents one such complementary technique. Habitats have distinct acoustic patterns, or soundscapes, as a result of their specific features and biological communities. Passive acoustic monitoring (PAM) presents a lower impact, innovative method to provide metrics for long-term monitoring of habitats. Marine soundscapes have not yet been described for the Wadden Sea; an ecosystem where reef habitats have experienced major changes over time due to various human-mediated impacts. This study provides a first catalogue of biotic acoustic signatures recorded at shellfish reef and neighbouring sand habitat in this ecosystem. Furthermore, recordings from natural reefs were compared to recordings from recently deployed artificial reefs, showing similar patterns of greater biotic acoustic diversity at the natural and artificial reefs compared to nearby sandflat. These results demonstrate that fine-scale differences in habitat soundscapes exist across reef habitats within a small geographic scale. This study provides the foundations for further quantitative research using PAM to monitor the Wadden Sea soundscape dynamics and understanding the role of sound in changing coastal ecosystem.

Biological sciences/Ecology/Ecosystem ecology

Earth and environmental sciences/Ocean sciences/Marine biology

reefs

soundscape

passive acoustic monitoring

coastal

Wadden Sea

Coastal ecosystems harbour highly productive habitats that provide specific ecological services to coastal communities, while also confronting various stressors and threats from human activities ^1,2. Monitoring of these marine habitats is therefore crucial to understanding impacts, managing activities, and protecting vulnerable species. However, the marine environment presents many challenges to biodiversity surveys, including the high effort and costs for manual or visual sampling and vessel operations. In addition, physical hurdles in coastal waters, such as variable visibility and light conditions for visual or video-based surveys, as well as harsh weather or hydrodynamic conditions, can preclude regular sampling. In areas of consistent high turbidity there is still a high reliance on (in some cases invasive) extractive sampling methods that often take irregular and seasonally biased snapshots of the biological communities³. Developing and testing non-invasive techniques that can collect data autonomously, at large scales with lower investment, is therefore of high priority to support effective management tools to protect coastal biodiversity. In this paper we provide a first baseline for passive acoustic monitoring (PAM) of temperate reefs in northern Europe. We show that PAM can provide an exciting and promising method to monitor coastal habitat characteristics under difficult conditions, providing continuous data on the acoustic activity and composition of marine communities.

Coastal habitats dominate marine soundscape studies, with much of the efforts to date concentrated on coral reefs ⁴, while temperate biogenic habitats (i.e. seagrass, kelp, and shellfish reefs) have received little to no attention in bioacoustic research ^4,5. To date, studies on temperate coastal habitats studies reported higher abundances of fish ^6,7 and mobile invertebrate sounds in structured coastal habitats compared to coastal areas lacking these.⁸

Our knowledge of the diversity of marine species that both produce and use sounds is rapidly growing. Sounds produced by marine organisms may be incidental, such as closing shells of bivalves,⁹ the movements of schooling fish,¹⁰ or feeding sounds (e.g. parrotfish or sea urchins)^11,12. However, sounds are also produced intentionally for communication, prey detection, or for navigation.^13,14

The initial identification of species using passive acoustic monitoring (PAM) often requires a visual confirmation by simultaneous camera captures, visual sightings or catch data of the sound-producing species (e.g. ¹⁵). For marine mammals, vocal repertoires have been relatively well described for the majority of species and acoustic identification based on sound alone is an established method in this field (e.g.,¹⁶). However, for most fish and invertebrate species, these acoustic baselines are still lacking.¹⁷ Documenting and cataloguing sound types and detections across coastal habitats is a key next step in developing PAM.¹⁸

Sound is a fundamental part of all ecosystems, and the specific physical features and ecological communities that comprise a habitat result in distinct acoustic patterns, or soundscapes.^6,19 Marine soundscapes may be indicative of biological activity at multiple levels.²⁰ Therefore, even where sounds produced cannot be identified to species, the perusal of acoustic signatures has been used to characterize the underwater soundscapes of marine habitats, e.g., reflecting community diversity and its fluctuations over space and time.^6,21,22

Here, we investigated the biological sound assemblages present on subtidal shellfish reefs and adjacent soft-sediment habitats in the western Dutch Wadden Sea. The Wadden Sea is a temperate shallow sea, fringing the southern border of the North Sea. To date, knowledge of the biological soundscape of the Wadden Sea is in its infancy with no prior research that the authors are aware of. We had two goals: 1) describing common biological underwater sound types of this shallow sediment dominated marine system; and 2) add to the body of soundscape research on temperate biogenic habitats, such as shellfish reefs, by comparing the diversity and abundance of underwater sound types to areas without biological structures (bare sand). We tested this by comparing sounds on a subtidal oyster reef and an adjacent bare area over time, and compared this with single samplings at another subtidal oyster reef and two nearby artificial reef sites to confirm both temporal and spatial consistency of effects.

2.1 Site description

The Wadden Sea is a vast temperate tidal soft-sediment dominated ecosystem composed of a mosaic of habitats, including intertidal flats, subtidal banks and gullies, shipwrecks, dykes, harbours, and other infrastructure. It also holds a number of natural shellfish reefs that are mainly intertidal in the present day as most subtidal biogenic reefs have experienced significant historical declines, including seagrass meadows, mussel beds (Mytilus edulis) and oyster reefs (historically Ostrea edulis, but now dominated by the introduced Magallana gigas).^23,24 These biogenic habitats provide important complex structures and support spawning, feeding and sheltering functions for fish and invertebrates,^25–28 and contribute to the coastal mosaic of habitats. Oyster reefs have been found to have distinct soundscapes from neighbouring habitats such as soft-sediment areas,⁸ making these areas a focal point for our investigation into habitat specific sounds and documenting biological sound types in the Wadden Sea. Compared to the intertidal areas of the Wadden Sea, subtidal habitats, and particularly the mobile communities that use these habitats, are an understudied aspect of this dynamic ecosystem.

Reef sound recordings used for this experiment were taken at four subtidal reefs in the in western Wadden Sea (Fig. 1). Natural subtidal oyster reefs are rare throughout the Dutch Wadden Sea. However, based on the local knowledge of fishermen,two oyster reefs that were permanently submerged in the Marsdiep tidal basin were identified (Nieuweschild, 53.06887, 4.88103; and Kornwerderzand: 53.09392, 5.20231). In addition, we could complement this with monitoring of two artificial reef assemblages made out of wood (recently deployed in the Eilandse Gat tidal basin in pyramids placed in blocks of 9; each pyramid approximately 3m³):²⁹ Keteldiep channel artificial reef: 53.222473, 5.012396 ; and Engelse Vaarwater channel artificial reef: 53.207747, 5.0389429 (Fig. 1A). Extremely turbid waters due to large amounts of mobile sediment lead to very low visibility throughout the Wadden Sea; this prevented the use of cameras or other visual methods to survey these sites.

2.2 Acoustic recordings

Recordings at subtidal reef sites were collected with hydrophones (SoundTrap 300STD; Ocean Instruments, NZ; sampling rate 24 kHz, set at high gain). Hydrophones were set to record continuously for two weeks. At each site, we recorded the sound simultaneously on the reef and at a paired off-reef control without any reef structures. The on-reef hydrophones were placed on top of the natural oyster reefs, or in the middle of the groups of artificial reef structures. The off-reef controls were placed at the same depth on the bare sand at a distance of 200m from each reef site.

Two deployment set-ups were used. At the oyster reefs, hydrophones were mounted in PVC frames (Fig. 1B) and were deployed using two anchors in the directions of tidal flow; a subsurface buoy ensured that the hydrophone was positioned approximately 1 m above the seafloor in water depths ranging from 2 to 5 m. At the artificial reef sites where tidal currents can be much stronger within the tidal channels, hydrophones were mounted onto heavy iron frames so that the hydrophone was positioned approximately 50 cm above the seafloor (Fig. 1C)

At the oyster reef Nieuweschild, recordings at the on and off reef locations were taken 6 times over a 2-year period; in April, June, August, and October 2021, and in June and October 2022. A concurrent recording was taken on and off the oyster reef Kornwerderzand in June 2022. At the two artificial reef sites continuous 3-day recordings were taken on and off the reefs at the end of September 2022 as part of a longer reef monitoring scheme.

2.3 Acoustic analyses

Recordings were manually inspected by the same observer (M.S.W) in RavenPro (Version 1.5, Cornell Lab of Ornithology, Ithaca, New York, USA), with the frequency window of 0–12kHz, and the time range of the view set at 5 minutes (using a Hann window of 512 samples at 50% overlap). Distinct biological sound types were coded in each recording. Due to the lack of previous works done in the area, sound type codes were developed iteratively, and naming conventions, where possible, based on previous biological sound typing work (e.g. drum, growl, grunt, knock etc.).³⁰

The most commonly found sound types that were identified as being of biotic origin were selected to use for this analysis (i.e. those that were detected > 50 times at all sites). Sound type presence was examined by calculating the proportion of 10-minute samples across the entire recordings in which each sound type was present (sensu ³¹).

2.3.1. Noise filtering

Tidal flow and wave noise had a high influence on background noise in recordings at all sites. Samples with high wave noise, rain, and current noise which had insufficient quality for the manual processing, were removed from the analyses. The threshold for excluding samples with ‘high’ noise levels was determined to be at an SPL of 110 dB by first selecting samples from recordings where manual analyses were determined through visual inspection to be “low”, “medium”, and “high” noise periods. The broadband means of these samples were analysed to show that these periods did indeed fall within distinct noise groups. The patterns of broadband noise also followed tidal cycles with slack water being the quietest. The actual detections of sound types within the recordings were then plotted against the broadband mean noise for each 10-minute recording period, where 99% of sound type detections fell below 110 dB. This led to removal of an average of 14% of 10-minute files per recording for the subsequent calculations of sound type presence.

2.3.2. Statistical analyses

Multivariate analysis of sound type proportions was used to investigate differences over time between the on and off reef sound types, and between daylight and overnight periods, at the Nieuweschild site. The test statistic was calculated using PERMANOVA (permutational multivariate ANOVA) with the proportion of 10-minute samples in which each sound type was present as the response variable; and a fully factorial combination of day vs night and on vs off reef as independent variables. Each of the six sampling periods was included as a replicate in the analysis. We also illustrated the differences visually by multidimensional scaling (MDS) plots. All multivariate analysis used Bray-Curtis dissimilarities as distance measures and the analysis was carried out in RStudio (Version 2023.09.1 + 494; ³²) using the vegan package.³³ We also tested the spatial consistency of the reef effect on sounds by calculating the proportion of total sound type presence in each recording at all four sites. From this we calculated the log response ratio of the reef effect (the natural logarithm of [the total proportion of sound registered on a reef divided by the total proportion of sound registered at their paired off-reef control]). The difference between sound proportions registered on reefs compared to their off-reef control were then tested statistically using a paired t-test and by calculating the confidence interval for the log-response ratio.

We found 11 biological sound types that were detected 50 or more times across the recording periods. These were categorized as Bubble-buzz, Chucks, Clicking, Drumming, Grunt, Growl-buzz, Horn, Knock, Knock-snap, Scraping, and Snap (Fig. 2). These 11 sound types were used for further analysis to inspect diurnal and seasonal patterns and to compare the on- with the off-reef habitats.

Across the 6 two-week recordings at the Nieuweschild site, we detected 3,405 individual biological sounds at the on-reef location, and 896 at the off-reef location. Eight sound types were most commonly detected on the reef: chucks, clicking, drumming, grunts, knocking, knock-snaps, scraping, and snaps, while three sound types were most commonly detected on the sand in the no-reef control: bubble-buzz, horns and growl-buzz (Fig. 3, Figure S1). The most common sound types detected at the on-reef station were scraping, snapping, and knocking (occurring in 1.7%±0.5, 2.3% ±0.6, and 1.3% ± 0.3 of the recorded 10-minute samples, respectively; mean ± se), while the horn sound type was most frequent at the off reef site (occurring in 1.8% ± 0.7 of the recorded 10-minute samples, mean ± se)(Fig. 3). There were significantly higher proportions of sounds detected on the natural oyster reef compared to the off-reef control over time at the site Nieuweschild (PERMANOVA: F_1,20=6.7, p < 0.001; Supplement 1). There was a trend towards a change in sound composition depending on day- or nighttime (PERMANOVA, effect of Day or Night: F_1,20=1.8, p = 0.073; Figure S2), with clicks more common during the night and chucks and horns more common during the day (Fig. 3). There were no significant interaction effects between on/off reef and day/nighttime (PERMANOVA: F_1,20=1.2, p = 0.287)

All four of the natural/artificial reef sites contained a higher proportion of samples with sounds than at their respective no-reef sand controls (paired t-test: n = 4, t = 3.2, p = 0.048; Figs. 4 & 5). The eleven selected sound types were, on average, detected 7 times more often on the reefs compared to their controls (log response ratio: mean = 1.94, ci = 1.65). Also, we found three additional sound types at the artificial reef sites in high abundances (more than 50 times). These were produced by the harbour Seal (Phoca vitulina): Growl, Pop, and Sneeze sounds (Figs. 2 & 5).

Understanding and mitigating the rapid changes taking place in coastal ecosystems requires monitoring techniques that give us insights into different aspects of marine communities. Biological soundscape monitoring offers a versatile tool to gauge the sounds present in specific ecosystems and how these vary spatially and temporally.^34,35 Temperate habitats and species have remained a relative gap in studies of soundscapes and descriptions of soniferous species compared to tropical counterparts.⁵ Here, we describe the most common biological sound types that characterised subtidal habitats in the western Dutch Wadden Sea; and we show that we can detect distinctly different sound type assemblages between sites. We also show that we can detect close-by differences in soundscapes between habitats by registering consistently higher proportions of sounds on subtidal reefs compared to neighbouring off-reef soft-sediment habitats. This provides the first descriptions of biological sound types and soundscape compositions in the Wadden Sea which will be a baseline for next steps in developing passive acoustic monitoring methods in the region. These results add to a growing body of soundscape studies that show habitats have distinct soundscapes due to their physical and biological make-up,⁸ and demonstrate that we can use PAM to detect short-range differences in subtidal biological activity.

Biological sound types were more abundant and diverse at the on-reef station than the neighbouring sand habitat at each of the reef sites. Crucial to these comparisons is the detection range of the sounds, i.e., to what extent were the sounds that were recorded on the reefs truly produced by organisms on the reef or could these also be acoustic spillovers from other nearby habitats. Shallow coastal environments have relatively short sound transmission distances - e.g. Biggs & Erisman (2021) found a transmission distance of a fish call to be between 44–281m in a very shallow estuary.³⁶ The water depths where our hydrophones were deployed were between 2–5 m, with on- and off-reef sites test pair distance of 200m. Differences in sound composition and lack of overlap between neighbouring on- and off-reef test pairs, indicated that soundscapes were qualitatively independent on this scale and reflected true small scale local soundscapes. Dedicated field tests with standardized signals are nevertheless needed and planned to solidify this.

We found a larger acoustic diversity and abundance at the on-reef station than the neighbouring sand habitat at each of the reef sites. This is consistent with findings that the fish and mobile invertebrate communities at reef sites in the Wadden Sea differ from neighbouring soft-bottom habitats.^29,37 Sound type diversity and abundances can also be indicative of community diversity,²² and of habitat status (Lamont et al. 2021).³¹ Extension from this groundwork and description of sound types will be to link these to the mobile communities at these habitats, and to build metrics from these that can support less invasive monitoring methods.

Several sound types were present across reef sites, as well as different sound types present between sites (e.g. the Growl-Buzz was not detected at the Nieuweschild reef, while Drumming was only detected at this site), indicating different levels of biological activity and composition. Inter-reef acoustic variability within a region was also identified by,⁸ and highlights some of the finer-scale variation in biological and physical reef characteristics that shape individual reef soundscapes. Some sound types were detected at both the artificial and the natural reefs, albeit in lower abundances at the artificial reefs. The artificial reefs, which had been deployed for 6 months at the time when the recordings were analyzed for this study, had detections of harbour seal sounds in higher abundances than the off-reef stations. That some biological sounds are consistent across subtidal reefs in this area suggests that sound type detections can add value to reef monitoring programs by contributing knowledge of habitat use and activity, as well as the impacts of human interventions and the progress of restoration programs.

These results build on several studies showing distinct acoustic patterns at coastal habitats - including tropical coral reefs,³⁸ temperate rocky reefs,¹⁹ as well as estuarine habitats comparable to those found in the Wadden Sea.^8,39,40 With the description of biological sound types, we can now look at longer-term patterns, including seasonal and annual patterns, which can also provide insights on potential sources. Furthermore, we can monitor long-term changes in the soundscape, and start building monitoring capacity.

Biological activity at reefs is usually highest overnight, and has been found to be reflected in soundscape patterns with higher sound pressure levels (SPL) and increased number of fish calling at dusk and dawn.^12,39 The patterns of sound types at the Nieuweschild station also showed trends toward day and night differences in sound type assemblages which may be linked to the species which are active during these periods. However, our recordings took snapshots at each habitat, and increased recording over seasons may further reveal diel patterns with changing behaviours such as species migration and spawning times.

The dynamic environment of the Wadden Sea also poses challenges to applying passive acoustic monitoring. There was a high influence of tidal current noise on detections, which was particularly evident at the artificial reef sites which are situated in tidal gullies that experience high current velocities (about 2.5 times higher maximum current speeds at the gullies than near to the Nieuweschild reef, unpublished data). Tidal effects on sound levels have been noted in other estuarine soundscapes, where high tide and falling tide periods have been observed to have greater biological sound levels, possibility also coinciding with better sound propagation at greater water depths.^41,42 These are important considerations for the descriptions of habitat soundscapes in this area, as well as planning for future development of monitoring schemes and recording cycles.

The field of marine ecoacoustics and descriptions of habitat soundscapes is growing rapidly. Sampling schemes and recording rates applied by studies of marine habitat soundscapes vary widely, as do methods applied for analyses of these recordings.³⁵ Several acoustic indices have been explored for describing aspects of biological communities in marine habitats,^43–48 or their utility in distinguishing between habitat types or describing habitat condition.^19,49,50 However, the application of these acoustic indices to recordings in marine environments has had mixed results.^{22,44,46,51,52} As reviewed and evaluated by Bohnenstiel et al. (2018), indices can be strongly influenced by particular sound events or a single species.⁵¹ To use passive acoustics as a monitoring tool, it is key to understand how soundscapes change relative to particular habitat characteristics and conditions and how these are reflected within sound metrics and indices. Documenting the sound assemblages which contribute to habitat soundscapes can inform us on how acoustic metrics may be influenced by different sources.

Compounding factors of the loss of ‘healthy’ habitat soundscapes as well as increasing levels of anthropogenic noise inputs to marine environments are resulting in changing marine soundscapes. Documenting current and potentially changing conditions in the ocean soundscape can provide important information for managing marine ecosystems.^53,54 Recognition of the importance of soundscapes, or the acoustic habitat, to marine life can shape management efforts toward soundscape conservation.⁵⁵ This first description of biological sound types at reef habitats in the subtidal Dutch Wadden Sea is a building block toward further development of soundscape monitoring in this ecosystem.

Author Contribution

M.S. Watson carried out the fieldwork, data collection and analyses, and writing. A.C.M Kok contributed to the analyses and writing. I. van Opzeeland contributed to the analyses and writing. B.D.H.K. Eriksson contributed to the statistical analyses and writing.

Acknowledgements

This research was funded by the Waddentools-Swimway Waddenzee project with financial contributions from the Waddenfund, the Ministry of Agriculture, Nature Management and Food Safety, and the Dutch provinces Noord-Holland, Groningen and Friesland. The authors thank Jaap and Hanneke Vegter, Jan Hottentot, Pieter Slik, and Jan Rotgans for their knowledge of the reefs, and assistance with deploying and collecting the hydrophones.

Data Availability

The data generated and/or analysed during the current study are not publicly available because they are still under analyses for another part of a PhD thesis but are available from the corresponding author on reasonable request.

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No competing interests reported.

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The biological soundscape of temperate reefs: characterizing natural and artificial reefs in the Dutch Wadden Sea

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Version 1

Abstract

Figures

Introduction

1. Methods

2.1 Site description

2.2 Acoustic recordings

2.3 Acoustic analyses

2.3.1. Noise filtering

2.3.2. Statistical analyses

2. Results

Discussion

Conclusion

Declarations

Author Contribution

Acknowledgements

Data Availability

References

Additional Declarations

Supplementary Files

Status:

Version 1