Soundscapes, the collection of sounds emanating from landscapes, convey important information about an environment and its biota. In the sea, different habitats have unique acoustic fingerprints (Butler et al., 2016) and within habitat types, soundscapes vary temporally (Radford et al., 2010) and spatially (Kennedy et al., 2010). Marine soundscapes are correlated with environmental (e.g., sea state, habitat depth) and biological parameters (e.g., coral cover, fish diversity and biomass; Piercy et al., 2014; Kaplan et al., 2017), and those acoustic signals are used by pelagic larvae to locate nursery habitats. Larvae that are attracted to soundscapes associated with settlement habitats include mobile species such as fish (Simpson et al., 2004; Parmentier et al., 2015) and decapod crustaceans (Stanley et al., 2012; Hinojosa et al., 2016), as well as sessile species like bivalves (Lillis et al., 2013, 2015) and corals (Lillis et al., 2016, 2018). Sound is different from other settlement cues (i.e., visual or olfactory cues) because it can carry information over long distances and is not affected by currents, turbidity, or light.

For sound to be a useful settlement cue, pelagic larvae must be able to detect it far from the source. Soundscapes of temperate rocky coastal reefs may be detected up to 10–25 km offshore by hydrophones (Cato and McCauley, 2002) and tropical coral reefs have been distinguished up to a few km (Piercy et al., 2014). As distance from the source increases, sounds are homogenized and the signal fades (Piercy et al., 2014). Given the limits of hearing capabilities of larvae, suitable habitats may only be detectable by larvae within a few hundreds of meters (Egner and Mann, 2005; Mann et al., 2007; Wright et al., 2010). Although many studies demonstrate the use of sound cues by fish and invertebrate larvae, the range at which they can detect and discriminate between cues is unclear.

Habitat degradation alters both the characteristics of the soundscape and the range of the signal. Soundscapes of degraded habitats (e.g., low coral cover, low fish diversity and biomass, loss of sponges) are often quieter and less complex than healthy habitats (Butler et al., 2016; Gordon et al., 2018). Lower soundscape amplitudes at the point of origin results in a smaller detection range (Piercy et al., 2014) and degraded soundscapes are less attractive to larval fish and invertebrates than soundscapes of healthy habitats (Butler, 2016; Gordon et al., 2018), likely hindering recovery of degraded areas.

Habitat restoration may restore marine soundscapes that act as settlement cues, but the detection range for cues from small restoration patches may be limited and preclude reestablishment of normal levels of larval settlement. In the Florida Keys, backreef hardbottom habitats are characterized by sponges, octocorals, and macroalgae. But cyanobacteria blooms have caused mass die-offs of sponges in a portion of Florida Bay leaving large swaths of barren habitat with few sponges and associated fauna (Butler et al., 1995; Herrnkind et al., 1997; Stevely et al., 2011). Previous studies have characterized backreef soundscapes and larval settlement in areas of healthy and degraded hardbottom habitat, as well as small patches of restored hardbottom habitats (Butler et al., 2016). Degraded hardbottom soundscapes are quieter and less complex than healthy hardbottom soundscapes and fewer larvae settle there. Although the soundscapes of restored patches of hardbottom are similar to those in healthy hardbottom, the abundance and diversity of larvae settling in restored patches is not the same as in healthy habitats (Butler, 2016). It is possible that the small size of the restoration patches may limit the transmission range of the restored soundscapes such that they do not propagate far enough to attract settling larvae.

In this study, we aimed to examine larval fish and invertebrate settlement at varying distances from broadcasted soundscapes from healthy hardbottom habitats. We hypothesized that healthy soundscapes would increase settlement over degraded soundscapes and settlement would decrease with distance from the sound source. To test this, we first determined the maximum range of detection of the auditory cue broadcast from an underwater speaker (i.e., where the signal to noise ratio was near zero). We then examined larval assemblages that settled on collectors placed at increasing distances from underwater speakers broadcasting healthy soundscapes at natural amplitudes, simulating a small, restored patch of habitat. Those results were compared to similar data wherein we broadcasted degraded soundscapes.

Underwater soundscapes are useful settlement cues for many larval fish and invertebrate species, but their usefulness depends on the range at which they can be detected (Radford et al., 2011). In this study, we examined sound propagation from an underwater speaker to determine the maximum potential range of detection by marine larvae that use sound to locate settlement habitat. We then compared the larval assemblages that settled on collectors placed both within and outside the detection radius of broadcasted soundscapes.

Results of the sound propagation experiment suggest that at natural amplitudes and calm surface conditions, healthy hardbottom soundscapes can be detected above natural soundscape conditions up to approximately 500 m from the source. However, under less ideal conditions (e.g., high winds, rainstorms) or where bottom type and depth are different, sound propagation is likely to differ. Collectors deployed at 1,000 m (more than double the ∼0 dB SNR range) were well outside the range of the speaker system, so settlement at those collectors was not affected by the soundscape treatment, as is probably the case for collectors at 500 m. The slightly higher number of larvae settling on collectors at 10 and 100 m from the broadcast source indicates a small effect of the broadcasted soundscape, although this effect is unlikely to be ecologically significant because differences in mean settlement and the composition of those larval assemblages were small (Figure 5 and Table 1).

The PERMANOVA indicated that larval assemblages differed between moon phases and mean settlement was greater during full moon overall, though this was likely driven by a few individual taxa, particularly the clam Lima. Marine organisms such as corals (Harrison et al., 1984; Brady et al., 2016) and fish (Farmer et al., 2017) use the lunar cycle to time the release of larvae, many of which settle around specific moon phases [fishes—bluehead wrasse (Victor, 1986); damselfish and surgeonfish (Sponaugle and Cowen, 1996), decapods—crabs (Cannicci et al., 2019), lobster (Acosta et al., 1997)].

The PERMANOVA results from our study indicated that there were community-level differences in larval assemblage between soundscapes. However, total larval settlement on collectors exposed to healthy soundscapes was only slightly higher than those exposed to degraded soundscapes and there was no effect of distance on larval settlement. Other studies have found soundscapes from nursery habitats are between 1.4 and 6.2 times more attractive to larvae than degraded soundscapes, non-settlement habitat soundscapes, or silent controls (Tolimieri et al., 2000; Leis et al., 2003; Simpson et al., 2004, 2008; Hinojosa et al., 2016). Healthy soundscapes can increase species-specific fish and invertebrate larval settlement by 1.4 to 4.8-fold (Simpson et al., 2005; Vermeij et al., 2010; Lillis et al., 2015, 2016, 2018; Gordon et al., 2018). But many studies on larval response to soundscapes are inherently biased because they were designed to test the response of larval taxa specifically chosen because they were suspected to respond to sound. That does not diminish the value of those studies, but they were not intended to randomly sample the planktonic meroplankton, as is the case for our study. Whether indicative of other habitats or not, we found that approximately 22% of the 41 taxa observed demonstrated a response to acoustic cues. For example, a fish (Paraclinus) and a gastropod (Turbo castanea) had higher settlement in response to broadcasted degraded soundscapes while two other gastropods (Bulla and Echinolittorina) and a bivalve (Lima) responded to healthy hardbottom soundscapes. However, responses were small for most of these taxa and given that approximately 78% of taxa collected had either no response to soundscapes or low abundance, sound may not be a particularly important settlement cue for most species in tropical hardbottom habitats.

Approximately 71% of the observed taxa had low settlement during the experiment (<50 individuals). Low settlement could indicate low larval supply, reflecting the degraded environment in which the experiment was conducted. If few larvae were present, their chances of encountering the small range of the broadcasted soundscapes was low and thus the effects of soundscape over distance were not likely to be detected. Low settlement could also reflect the type of larval collector we deployed. The collectors used in this experiment were designed to mimic benthic algae commonly used as settlement habitat by many organisms within hardbottom habitat, but taxa that prefer different settlement substrates may have avoided the collectors. Additionally, collectors were suspended vertically in the 2–4 m deep water column rather than directly on the bottom to prevent colonization by mobile benthic organisms. Also, highly mobile organisms such as fish, could have abandoned the collector prior to collection. Although the collectors appeared to be adequate for capturing some benthic fish species such as the blenny Paraclinus, other common backreef fishes were rarely caught (e.g., Haemulon, Opsanus) or not caught at all (e.g., Lutjanus, Calamus). Larval fish supply to the Florida Keys is lowest in late fall (D’Alessandro et al., 2007) which could also account for the low numbers of fish larvae that we observed in our summer-fall study period.

Larvae have available to them a variety of settlement cues and some species utilize multiple cues to locate nursery habitat (e.g., Eastern oyster, Crassotrea virginica; Turner et al., 1994; Lillis et al., 2013; blue crab, Callinectes sapidus; Tankersley et al., 1995; horseshoe crab, Limulus polyphemis; Medina and Tankersley, 2010). This experiment may thus have missed larvae that use sound in addition to other settlement cues such as olfaction.

Because the degraded soundscapes were broadcast at natural amplitudes there should be little difference in soundscape (Butler et al., 2016) or settlement between collectors inside and outside the range of the broadcast. Yet, a few genera were collected in greater numbers within the range of degraded soundscapes (e.g., Paraclinus, Turbo) than outside the range of the speaker system. This indicates that there is a difference between broadcasted degraded soundscapes and natural degraded soundscapes for at least some settlers. Although soundscapes were broadcasted at ecologically relevant, natural amplitudes there are artifacts of playback that alter the properties of the soundscapes. For example, the speaker frequency response drops off drastically below 200 Hz, so frequencies below 200 Hz in the hardbottom soundscape would not have been broadcast as loudly as they were recorded.

Taxa found in greater numbers within range of the degraded soundscapes may also prefer different nursery habitat types or were avoiding healthy hardbottom soundscapes. For example, Simpson et al. (2011) found that taxa with pelagic or nocturnally active lifestyles, avoided reef soundscapes. Healthy hardbottom soundscapes are naturally louder and more complex (Butler et al., 2016) and the soundscapes we broadcasted reflected that. Louder, more complex soundscapes could indicate a larger biological community and potentially more predators. Unfortunately, the preferred nursery habitats for most of the more than 40 taxa observed in this study are unknown.

A few taxa had contradictory settlement patterns. For example, the shrimp genus Palaemonetes, had high settlement during new moon on degraded soundscape collectors and on healthy soundscape collectors during full moon (Figures 7G,H). We were unable to identify this genus to species and it is possible that more than one species was collected, each with contrasting settlement patterns. This highlights the need to look more deeply at the settlement preferences of Palaemonetes and other taxa with inconsistent settlement patterns.

Much of the variation in larval settlement, such as the high settlement of Lima at two 1,000 m collectors, may be due to random factors such as local currents, habitat structure, or time period. Though not designed as a factor of interest in the experiment, site and collection date were random factors that were correlated (one pair of sites were used for a consecutive full and new moon period, or one “collection period”) and could have affected larval settlement. As site and date were intrinsically linked in this experiment, it was not possible to explore the individual contributions of these factors, but both are likely to contribute to the observed variation in larval settlement and community assemblage since larval settlement varies temporally (e.g., on diel, lunar, and seasonal cycles) and spatially (O’Beirn et al., 1996; Acosta et al., 1997, Martínez and Navarrete, 2002; D’Alessandro et al., 2007) for many species.

Given the small range of the broadcasted soundscapes that we measured, the soundscapes of small patches of healthy hardbottom habitat likely have a very limited range. This restricted range of sound propagation has implications for restoration efforts. Previous work in Florida Bay found greater larval settlement within healthy habitats than in degraded habitat (Butler, 2016). But within small (25 m × 25 m) hardbottom patches, where the sponge community and soundscape had been restored, larval settlement did not match natural healthy hardbottom levels (Butler, 2016). Though the soundscape had been restored within these small patches, they were essentially a point source and therefore had a much smaller range of detection than the large area of healthy habitat (Radford et al., 2011; Piercy et al., 2014). More larvae were potentially able to detect the sounds of natural healthy habitat at greater distances and could explain why Butler (2016) did not see comparable settlement in restored patches and healthy hardbottom areas. Our results indicate that the range for a small point source of healthy hardbottom soundscape is a few hundred meters but the effective detection range for larvae is likely much smaller.

While it is possible to restore soundscapes to natural levels, the small patch size of many restored sites may limit the range of the acoustic settlement cue, negating its effectiveness as a settlement cue for larvae and hindering ecological recovery. Future work should examine what acoustic range or level of acoustic connectivity between patches is necessary to restore the settling larval assemblage. A larger patch will have a larger detection range but several small patches within range of each other may extend that detection range with fewer resources. Patches close to large areas of healthy hardbottom may benefit from spill-over, being near a potential source of larvae or colonizing animals but the greater detection range may draw more larvae to the natural healthy habitat at the expense of the restored patch. Restoration patch size, patch connectivity, and patch location are well studied concepts in other ecosystems (Schultz and Crone, 2005; Fink et al., 2009; Morrison et al., 2010; Gittman et al., 2018) but have not yet been explored in hardbottom habitats.

The results from this study adds to the growing body of literature investigating soundscapes as settlement cues for marine larvae. Our results suggest that sound alone may not be an important settlement cue for many larvae in hardbottom habitats and that sound emanating from a point source at natural levels has a relatively small range of attraction and may not have the necessary range to draw in larvae over long distances. Single, small point sources, such as small restoration patches, may not be effective at restoring settlement to the same level as large areas of healthy habitat. However, sound is just one cue that larvae use to locate and choose settlement habitat and should be considered in conjunction with other settlement cues.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The animal study was reviewed and approved by Old Dominion University Institutional Animal Care and Use Committee.

EA and MB funded the research. EA performed the research and analyses with guidance from MB and JB and wrote the initial manuscript with revisions made by MB and JB. All authors designed the study.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.