Marine invertebrate larvae were once considered passive particles lacking the ability to detect or respond to their environment (G. Thorson, 1950; Chia et al., 1984) but it is now widely accepted that interactions between both environmental conditions and biologically-generated cues affect larval behavior and physiology across many marine invertebrate taxa, including corals (Rodriguez et al., 1993; Shanks, 2009; Gleason and Hofmann, 2011) (Table 1). The ocean was once described as ‘The Silent World’ by Cousteau and Dumas in 1953, but we now know that coral reefs are bioacoustically rich. Many reef inhabitants produce sound during a wide array of behaviors which together contribute to the ambient soundscape of the “choral” reef (Schmitz, 2002; Lobel et al., 2010; Lobel, 2013; Radford et al., 2014a). This ambient soundscape has been shown to act as an orientation cue for the pelagic larvae of many fish, decapod crustaceans and reef-building corals, assisting their orientation towards suitable settlement sites (Tolimieri et al., 2000; Tolimieri et al., 2002; Jeffs et al., 2003; Simpson et al., 2004; Leis and Lockett, 2005; Simpson et al., 2005; Montgomery et al., 2006; Vermeij et al., 2010; Radford et al., 2011).

Reef-building corals represent keystone species in coral reef ecosystems, providing valuable ecosystem goods and services to 100s of millions of people (Woodhead et al., 2019). However, the behavioral responses of coral larvae (planulae) to acoustic stimuli and the sensory mechanisms by which they detect acoustic cues remain poorly understood. Yet, these are of increasing importance, especially in the context of growing anthropogenic pressures on coral reefs, including climate change, overfishing, sewage and fertilizer runoff and noise pollution (Lecchini et al., 2018; Richmond et al., 2018; Jones, 2019; Duarte et al., 2021). Coral larvae can respond to an array of environmental cues that guide their settlement. We review these, with a particular emphasis on acoustics and soundscapes, the importance of which is just recently coming to light.

The grinding and popping of foraging echinoids, grazing scarids, vocalizing fish and snapping shrimp all contribute to the biophony of coral reefs (Simpson et al., 2004; Simpson et al., 2008; Lobel et al., 2010; Lobel, 2013; McWilliam et al., 2017). Thus, higher quality, healthy coral reefs are significantly louder, richer in acoustic events and more acoustically complex than degraded reefs (Piercy et al., 2014; Bertucci et al., 2016; Freeman and Freeman, 2016; Gordon et al., 2018). Acoustic cues are particularly useful for aquatic animals as sound travels faster and further underwater relative to other sensory cues, irrespective of directional currents (Urick, 1983; Ainslie, 2010; Duarte et al., 2021). Many marine invertebrates, therefore, have evolved the ability to detect and respond to acoustic cues, most likely by using specialized receptors (Salmon and Horch, 1973; Popper et al., 2001; Schmitz, 2002; Kaifu et al., 2008; Mooney et al., 2010; Vermeij et al., 2010; Wilkens et al., 2012; Lillis et al., 2013; Edmonds et al., 2016; Lillis et al., 2016; Solé et al., 2016; Vazzana et al., 2016; Charifi et al., 2017; Wale, 2017; Jézéquel et al., 2018; Lillis et al., 2018), and many taxa demonstrate increased rates of larval settlement in the presence of acoustic cues and during louder levels of acoustic cues (Jeffs et al., 2003; Simpson et al., 2004; Simpson et al., 2005; Stanley et al., 2010; Simpson et al., 2011; Stocks, 2012; Stanley et al., 2012a; Stanley et al., 2012b; Lillis et al., 2013; Lillis et al., 2015; Hinojosa et al., 2016).

Acoustic cues can also influence the swimming orientation and settlement behavior of coral larvae. In an in situ settlement chamber experiment, larvae of the Caribbean scleractinian coral Orbicella faveolata (previously Montastraea faveolata) exhibited directed phonotaxis, with larvae moving towards the source of a broadcasted coral reef soundscape irrespective of chamber orientation (Vermeij et al., 2010). In a separate study, O. faveolata larvae exhibited higher settlement rates when exposed to soundscapes from louder, more diverse coral reefs when compared to soundscapes from two quieter reefs characterized by either sponges and coral rubble or industrial debris and algal growth. (Lillis et al., 2016). These findings imply that the elevated acoustic power associated with more diverse habitats, or the absence or presence of specific frequencies within healthier habitats, may lead to increased larval settlement. The same authors found that settlement rates in larvae of the reef-building coral Porites astreoides doubled in an acoustic environment with higher levels of low-frequency sound, which are typical of a healthier reef with higher coral cover and higher densities of fish (Lillis et al., 2018). This suggests that low-frequency sounds are the predominant drivers of response in this species, and that the absence of these low frequencies may reduce settlement.

High-frequency sounds attenuate more rapidly underwater, but lower-frequency sounds emanating from reefs are theoretically detectable to invertebrates within 500 m from the source (Rogers and Cox, 1988; Anderson et al., 2021). However, currents and fluid flows may limit the ability of larvae to successfully navigate to cues 500 m away; therefore in practice, the range of detection and successful response may be closer still to 10 – 100 m (Gleason and Hofmann, 2011). Although O. faveolata larvae exhibit directional phonotaxis in situ (Vermeij et al., 2010), the experimental confinement to an acrylic chamber likely restricted fluid flow, allowing larvae to move unimpeded by currents. Therefore, our understanding of the spatial scale at which coral larvae are able to detect acoustic stimuli in their natural environment is still limited. The difficulties associated with in situ settlement experiments in complex topographical and hydrodynamic environments both highlights the challenge of interpreting the ecological significance and restoration utility of experimental results (Hata et al., 2017; Mayorga-Adame et al., 2017; Randall et al., 2020; Levenstein et al., 2022) as well as the many considerations that must be made when deisgning future acoustic larval settlement experiments.

To date, most studies of phonotaxis in coral planulae have been conducted with larvae from broadcast spawners (but see Lillis et al., 2018), therefore larvae from brooding corals are relatively understudied. However, it is proposed that mechanosensory epidermal cilia are responsible for auditory perception in coral (Vermeij et al., 2010). Therefore, given the abundance of dense cilia found on their surface, brooded larvae are also expected to possess the sensory mechanisms to detect and respond to acoustic stimuli (Gleason and Hofmann, 2011). This hypothesis requires further testing.

Sonic vibrations in water have both pressure and particle motion components (Reviewed in Nedelec et al., 2016). In their adult stages, most aquatic invertebrates can detect the particle motion component of sound, using specialized organs such as mechanosensory setae, chordotonal stretch receptors between the joints of appendages and statocyst and statolith receptor systems (Popper and Fay, 1999; Popper and Lu, 2000; Popper et al., 2001; Bleckmann, 2004; Nedelec et al., 2016). Many invertebrate larvae, including those of cnidarians, have a diversity of cilia-based mechanosensory systems that function during feeding, locomotion, tactic response, predator–prey interactions and settlement (Chia and Crawford, 1977; Chia and Koss, 1979; Freeman and Ridgway, 1990; Marlow et al., 2009; Bezares-Calderón et al., 2020), with many of these systems sensitive to acoustic particle motion (Tranter et al., 1982; Rogers and Cox, 1988; Budelmann, 1992; Kennedy et al., 1996; Zhadan, 2005; Tran and Hadfield, 2013; Lillis et al., 2015).

The sensory mechanisms employed by coral larvae to detect acoustic stimuli, however, remain unknown. Early studies of the temperate reef-building coral-species Balanophyllia regia and the tropical coral species Pocillopora damicornis demonstrated that the larval ectoderm is primarily composed of flagellated collar cells - a single flagellum surrounded by a ring of microvilli (Lyons, 1973; Vandermeulen, 1975). While the main function of these cells are primarily thought to be calcification, phagocytosis of food particles and motility, it has been suggested that these cells may also have a sensory function. This assumption was based on their similarities with statocyst systems used in the detection of acoustic cues in other invertebrate taxa (Lyons, 1973).

The laser Doppler vibrometry (LDV) method relies on the detection of the Doppler frequency shift that occurs when light is dispersed by a moving surface (Rothberg et al., 2017). In a study exploring particle motion detection in marine invertebrates, LDV was used to measure whole body vibrations (displacement, velocity and acceleration) as a putative stimulus of statocyst organs in cuttlefish (Family Sepiidae) and scallops (Family Pectinidae) (André et al., 2016). This experiment piloted the use of LDV techniques in an underwater bioacoustics study and highlights its potential value for use across other marine invertebrate taxa. LDV has also been successfully used to measure the mechanical response of microstructures such as antennae and sensory hairs to electrical and sound stimuli in several terrestrial invertebrates (Göpfert et al., 1999; Göpfert and Robert, 2002; Sutton et al., 2016). Although it is evident that coral larvae both respond to acoustic cues and possess the mechanosensory structures capable of detecting particle motion (Vermeij et al., 2010; Lillis et al., 2016; 2018) (Figures 1C, D), to date there have not been any attempts to measure the mechanical responses of their exterior cilia-based sensory systems to acoustic cues in a bioacoustics study, nor has this been done for the larvae of any marine invertebrate. We propose that laser Doppler vibrometry could be broadly applied to investigate the mechanosensory ability of coral larvae epidermal cilia, including quantifying both cilia beat dynamics and frequency-specific sensitivity to incident particle velocity. Using analytical signals capturing the spectral diversity of samples from coral reef sound recordings, and playbacks of the recordings themselves, it will be possible to determine the auditory sensitivity and bandwidth of coral larvae, offering a mechanistic basis for their phonotactic behavior (Figures 1A, B).

Coral reef soundscapes play an important role in coral larval orientation, habitat location, settlement and recruitment, ultimately affecting reef growth and resilience (Vermeij et al., 2010; Lillis et al., 2016; Lillis et al., 2018). However, with many coral reefs subject to degradation through climate change, overfishing and pollution, reef soundscapes are changing (Spalding and Brown, 2015; Hughes et al., 2017; Hughes et al., 2018; Duarte et al., 2021). For example, between 2012 and 2016, cyclones and intense bleaching meant the Great Barrier Reef experienced the most severe degradation period in recorded history (Hughes et al., 2017). As a result, soundscapes were negatively impacted across four complementary ecoacoustic indices; they were on average 15 dB SPL re 1 µPa quieter and had significantly reduced acoustic complexity, richness and rates of snapping shrimp (Family Alpheidae) snaps (Gordon et al., 2018).

In light of the ecological crisis on coral reefs, novel restoration techniques are becoming increasingly important in the conservation and restoration of these ecosystems. One promising new tool is acoustic enrichment, whereby recordings from relatively healthy coral reefs are played back through underwater speakers (Gordon et al., 2019). This approach has been demonstrated to improve metrics of fish community health in degraded coral reef habitat on an experimental scale (Gordon et al., 2019). Over the natural fish breeding season on the Great Barrier Reef (November-December), this study showed that reefs with acoustic enrichment had increases in fish recruitment across multiple trophic guilds, a doubling in overall fish abundance, and a 50% increase in species richness (Gordon et al., 2019). A subsequent study found that successful management and restoration of coral reefs leads to the recovery of the natural soundscape; maturing restoration projects in Sulawesi exhibited similar levels of acoustic richness to healthy reefs (Lamont et al., 2021).

Recent coral reef restoration efforts have focused on increasing population sizes, genetic diversity and the natural adaptive capacity of corals, for example, through fragment rescue, asexual propagation, in situ and ex situ coral nurseries and sexual propagation in order to mitigate reef degradation caused by climate change and local stressors (Heyward et al., 2002; Cruz and Harrison, 2017, dela Cruz and Harrison, 2020; Suzuki et al., 2020; Randall et al., 2020; Vardi et al., 2021; Harrison et al., 2021; Baums et al., 2019, 2022). In addition, coral breeding efforts in land-based facilities continue to scale up (Craggs et al., 2017; Craggs et al., 2020; O’Neil et al., 2021) while virtually all coral propagation programs seek more efficient ways to induce coral settlement in large numbers without introducing potentially detrimental competing organisms (Randall et al., 2020). Acoustic enrichment can be used in conjunction with all of these newer, breeding-based restoration techniques to help increase settlement rates, population growth and species diversity. By boosting coral settlement at restoration sites, short term acoustic enrichment will also help to restore natural acoustic complexity and phonic richness, thus further accelerating and reinforcing reef recovery.

Current examples of acoustic enhancement in reef restoration include 'The Reef Song Project', an Australian Coral Reef Resilience Initiative (ACRRI) undertaken in association with the Australian Institute of Marine Science (AIMS). This project is the first to investigate the efficacy of acoustic enrichment in situ. Using healthy reef recordings to attract fish communities to sixty patch reefs made of coral rubble and live fragments at Ningaloo Reef and the Great Barrier Reef in Australia, this five-year initiative is primarily exploring the roles of fish husbandry and herbivory on coral growth and reef recovery. Using photogrammetry, coral growth will be monitored over time (Australian Institute of Marine Science, 2023). Additionally, the Woods Hole Oceanographic Institute (WHOI) have developed the ‘Reef Solutions Initiative’. Following the discovery by WHOI scientists that coral larvae are attracted to the soundscapes of healthy reefs (Lillis et al., 2016; Lillis et al., 2018), this initiative seeks to incorporate acoustic enrichment into intervention strategies to help corals repopulate degraded reefs (Woods Hole Oceanographic Institute, 2023). To improve our understanding of the reef recovery process and the impact of reef restoration, the application of low-cost, low specification passive acoustic monitoring in combination with machine-learning analysis may be applied to improve the analysis of ecoacoustic indices and successfully track coral reef restoration (Lamont et al., 2022; Williams et al., 2022).

In sum, acoustic enrichment is a promising tool for coral reef restoration due to its demonstrated efficacy across multiple taxa, yet its potential is still largely untested. Restoring keystone species and re-establishing complex interspecific interactions can promote successful management and restoration of coral reef ecosystems. Reef-building scleractinian corals are keystone species and it is their three-dimensional structure on which all coral reef life forms depend for food, sanctuary and survival. In order to fully assess the potential of acoustic enrichment and effectively apply this method as a reef restoration tool, we must continue to explore how different coral taxa respond to acoustic cues while gaining a better understanding of the mechanisms by which coral larvae sense their acoustic environment. This will also allow us to effectively place acoustics within the hierarchy of sensory cues that coral larvae integrate to locate an optimal site for settlement and recruitment to the reef.

JP, EW and SDS conceived the idea for this mini-review. JP wrote the manuscript. All authors listed made substantial contribution to the discussion of ideas outlined in the work and the development of the manuscript. All authors contributed to the article and approved the submitted version.