Acoustic enrichment can enhance fish community development on degraded coral reef habitat

Coral reefs worldwide are increasingly damaged by anthropogenic stressors, necessitating novel approaches for their management. Maintaining healthy fish communities counteracts reef degradation, but degraded reefs smell and sound less attractive to settlement-stage fishes than their healthy states. Here, using a six-week field experiment, we demonstrate that playback of healthy reef sound can increase fish settlement and retention to degraded habitat. We compare fish community development on acoustically enriched coral-rubble patch reefs with acoustically unmanipulated controls. Acoustic enrichment enhances fish community development across all major trophic guilds, with a doubling in overall abundance and 50% greater species richness. If combined with active habitat restoration and effective conservation measures, rebuilding fish communities in this manner might accelerate ecosystem recovery at multiple spatial and temporal scales. Acoustic enrichment shows promise as a novel tool for the active management of degraded coral reefs.


Statistics
For all statistical analyses, confirm that the following items are present in the figure legend, table legend, main text, or Methods section.

n/a Confirmed
The exact sample size (n) for each experimental group/condition, given as a discrete number and unit of measurement A statement on whether measurements were taken from distinct samples or whether the same sample was measured repeatedly The statistical test(s) used AND whether they are one-or two-sided Only common tests should be described solely by name; describe more complex techniques in the Methods section.
A description of all covariates tested A description of any assumptions or corrections, such as tests of normality and adjustment for multiple comparisons A full description of the statistical parameters including central tendency (e.g. means) or other basic estimates (e.g. regression coefficient) AND variation (e.g. standard deviation) or associated estimates of uncertainty (e.g. confidence intervals) For null hypothesis testing, the test statistic (e.g. F, t, r) with confidence intervals, effect sizes, degrees of freedom and P value noted Give P values as exact values whenever suitable.

For Bayesian analysis, information on the choice of priors and Markov chain Monte Carlo settings
For hierarchical and complex designs, identification of the appropriate level for tests and full reporting of outcomes Estimates of effect sizes (e.g. Cohen's d, Pearson's r), indicating how they were calculated Our web collection on statistics for biologists contains articles on many of the points above.

Software and code
Policy information about availability of computer code

Data collection
No software was used for data collection in this study.

Data analysis
All figure creation and statistical modelling was conducted in R v. 3.5.0. Figures were prepared using the packages cowplot, ggmap and ggplot2. Statistical modelling was conducted using the packages lme4 and mgcv. Acoustic recordings were analysed using the paPAM and PAMGuide packages on MATLAB.
For manuscripts utilizing custom algorithms or software that are central to the research but not yet described in published literature, software must be made available to editors/reviewers. We strongly encourage code deposition in a community repository (e.g. GitHub). See the Nature Research guidelines for submitting code & software for further information.

Data
Policy information about availability of data All manuscripts must include a data availability statement. This statement should provide the following information, where applicable: -Accession codes, unique identifiers, or web links for publicly available datasets -A list of figures that have associated raw data -A description of any restrictions on data availability Raw data are available from the University of Exeter's institutional repository.

nature research | reporting summary
October 2018 Field-specific reporting Please select the one below that is the best fit for your research. If you are not sure, read the appropriate sections before making your selection. All studies must disclose on these points even when the disclosure is negative.

Study description
Thirty-three experimental coral-rubble patch reefs were constructed on Australia's northern Great Barrier Reef. Each reef was assigned randomly to one of three treatments in an independent-measures design, within the constraints that there were equal numbers of reefs in each treatment and the same treatment was never allocated to reefs that were spatially adjacent. The three treatments were soundscape-restored reefs (healthy soundscapes broadcast from loudspeakers overnight), dummy-loudspeaker reefs (a silent loudspeaker replica attached to the reef in the same way as loudspeakers), and no-loudspeaker reefs. Developing fish communities on each reef were monitored for 40 days, with juvenile damselfishes surveyed regularly throughout the 40 days, and the entire juvenile fish community surveyed once at the end of the 40 days.

Research sample
Communities of juvenile damselfishes associated with 33 experimental coral-rubble patch reefs (n = 11 for each treatment) were sampled throughout the experimental period; damselfishes were chosen for this as they are non-cryptic, highly abundant (up to 50% of reef fish communities) and possible to visually survey accurately with minimal disturbance to the developing fish community. Full community surveys of all juvenile fishes associated with the same reefs were carried out at the end of the experimental period (33 reefs, n = 11 for each treatment).

Sampling strategy
Experimental coral-rubble reefs were built in sandy areas of 2-4.5 m depth, at a minimum of 100 m from each other. The minimum distance between reefs was first chosen based on measurements of loudspeaker playback acoustic propagation in both soundpressure and particle-motion domains. Having determined this, the maximum possible number of experimental reefs in the space available at the field site was 33 (n = 11 per treatment); this was therefore the sample size.

Data collection
For surveys of damselfishes throughout the experiment, visual surveys by a SCUBA diver (T.A.C.G.) were carried out, with the observer and dive buddy maintaining a distance of at least 1 m from the reef during surveys in order to minimise disturbance to the community. For surveys of the whole community at the end of the experiment, each reef was surveyed by the observer (T.A.C.G.) dismantling the reef piece-by-piece, checking each piece of rubble thoroughly and using dilute clove oil and a hand net to capture all juvenile fishes on the reef. All fishes were identified to species, except in cases where uncertainty meant that identification was only possible to family or sub-family level. In both cases, data were recorded on a dive slate.
Timing and spatial scale All reefs were constructed between 27 October and 5 November 2017. Forty-day survey periods were started for each reef immediately after construction, with final community surveys taking place between 6 December and 15 December. Regular surveys of damselfishes (family Pomacentridae) were carried out throughout the 40-day period; each reef was surveyed 10 times, with between 3-9 days between consecutive surveys. Each reef was a minimum of 100 m from its nearest neighbour, with all reefs placed on sand flats in water depth of 2-4.5 m in the lagoonal waters south and south-west of Lizard Island Research Station.

Data exclusions
No data were excluded from the final whole-community analyses or the regular damselfish surveys. In the trophic-level analyses, corallivores made up less than 0.25% of all fish, and were found on only two of 33 reefs; due to a lack of statistical power, they were therefore not analysed as a separate trophic group in the manner that other groups were (herbivores, piscivores, planktivores etc.).

Reproducibility
This experiment is the first to use this methodology for long-term community development surveys. However, short-term deployment of patch reefs using the same protocol is a well-established method in the literature, and has been experimentally replicated many times (

Randomization
Loudspeaker treatment was allocated randomly to experimental reefs, but constrained such that there were equal numbers of reefs in each treatment, and the same treatment was never allocated to reefs that were spatially adjacent. Within the soundscaperestoration treatment, five different playback tracks were used to reduce pseudoreplication, with each track being allocated to soundscape-restoration reefs at random (each recording was allocated to 2-3 of the 11 soundscape-restored reefs). Playback track ID was included as a random term in linear mixed model and generalised linear mixed model analyses.

Blinding
It was not possible to be blind to the experimental treatment during surveys, as field surveys were carried out in situ on reefs where the loudspeaker, dummy loudspeaker or absence of loudspeaker was evident to the surveyor.
Did the study involve field work?

Yes No
Field work, collection and transport

Field conditions
Weather conditions were calm during the experiment; on 88% of the days, wind speeds were less than 15 knots, on the remaining 12% of days, wind speeds were between 15 and 30 knots. Sea state was always 0-2 on the Beaufort scale. As all different treatments were being run simultaneously, any variation in weather conditions would be experienced equally by all treatments.