Oyster larvae settle in response to habitat-associated underwater sounds

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Abstract

Following a planktonic dispersal period of days to months, the larvae of benthic marine organisms must locate suitable seafloor habitat in which to settle and metamorphose. For animals that are sessile or sedentary as adults, settlement onto substrates that are adequate for survival and reproduction is particularly critical, yet represents a challenge since patchily distributed settlement sites may be difficult to find along a coast or within an estuary. Recent studies have demonstrated that the underwater soundscape, the distinct sounds that emanate from habitats and contain information about their biological and physical characteristics, may serve as broad-scale environmental cue for marine larvae to find satisfactory settlement sites. Here, we contrast the acoustic characteristics of oyster reef and off-reef soft bottoms, and investigate the effect of habitat-associated estuarine sound on the settlement patterns of an economically and ecologically important reefbuilding bivalve, the Eastern oyster (Crassostrea virginica). Subtidal oyster reefs in coastal North Carolina, USA show distinct acoustic signatures compared to adjacent off-reef soft bottom habitats, characterized by consistently higher levels of sound in the 1.5-20 kHz range. Manipulative laboratory playback experiments found increased settlement in larval oyster cultures exposed to oyster reef sound compared to unstructured soft bottom sound or no sound treatments. In field experiments, ambient reef sound produced higher levels of oyster settlement in larval cultures than did off-reef sound treatments. The results suggest that oyster larvae have the ability to respond to sounds indicative of optimal settlement sites, and this is the first evidence that habitat-related differences in estuarine sounds influence the settlement of a mollusk. Habitat-specific sound characteristics may represent an important settlement and habitat selection cue for estuarine invertebrates and could play a role in driving settlement and recruitment patterns in marine communities.

Figures

  • Figure 1. Map of Pamlico Sound, NC. Oyster reserves at which sound recordings were made are marked (CH = Crab Hole; WB = West Bay). Fieldbased settlement experiment was conducted in West Bay. doi:10.1371/journal.pone.0079337.g001
  • Figure 2. Larval settlement experiment (Laboratory) setup. a) Side view schematic diagram of a replicate experimental tank (0.25 m60.5 m) used in lab-based settlement experiment 1, showing the placement of a submerged speaker and container housing oyster larvae within a water bath, and b) Cylindrical treatment tank (20-L, 0.3 m water depth) used in lab experiment 2 containing an underwater speaker and five larval culture jars containing groups of actively swimming larvae. Larger view of larval culture jars with and without substrate is shown. No additional substrate was provided in experiment 1 and 2a; oyster shell discs were placed in the bottom of containers in experiment 2b. doi:10.1371/journal.pone.0079337.g002
  • Figure 3. Larval settlement experiment (Field) setup. a) Map of field experiment site in West Bay. Circles denote locations of ‘‘off-reef’’ replicates, and squares are ‘‘reef’’ replicates. The extent of the West Bay oyster reserve is indicated by the box bordering the reef replicates. Inset shows experiment location in West Bay, b) Schematic of the larval housing placed at each replicate in off-reef sites and c) in the reef site. Larval cultures were suspended at 1 m above the seabed at each location, with the two habitats providing the ambient sound treatments. doi:10.1371/journal.pone.0079337.g003
  • Figure 5. Spectral composition of sound in experiment 1 tanks (reef sound and no sound (control) treatments). The black line represents the spectrum of the original in situ recording from West Bay oyster reserve that was replayed in reef sound tanks. Power spectral density estimated via Welch’s method (Hamming window, 1-sec averages with 50% overlap). doi:10.1371/journal.pone.0079337.g005
  • Figure 4. Oyster reef and off-reef acoustic spectra for two Pamlico Sound sites. Power spectral density for sounds recorded on and offreefs taken monthly July-September at (a) West Bay and (b) Crab Hole. Because the field recordings differed in total length, each multi-hour recording was shortened to a one-hour sample that began at sunset.This produced six pairs of recordings collected simultaneously in each habitat type. The displayed data represent the median spectra for each hour-long sample calculated from a series of non-overlapping 10-sec duration windows. doi:10.1371/journal.pone.0079337.g004
  • Figure 6. Spectral composition of one set of original and replayed sounds used in lab experiment 2. a) Reef and off-reef sounds recorded simultaneously in West Bay, NC in July 2010. b) Comparison of in situ off-reef sound, replayed off-reef sound in experimental tank and no sound tank spectra. c) Comparison of in situ reef sound, replayed reef sound in experimental tank and no sound tank spectra. Power spectral density estimated via Welch’s method (Hamming window, 1-sec averages with 50% overlap). doi:10.1371/journal.pone.0079337.g006
  • Figure 7. Mean oyster settlement in reef sound and no sound treatments for laboratory experiment 1 trials. Settlement was measured as proportion of larvae settled in a culture at the termination of a trial. Error bars represent 1 S.E. N = 28. doi:10.1371/journal.pone.0079337.g007
  • Figure 8. Mean oyster settlement in reef sound, off-reef sound and no sound treatments for experiment 2 trials with a) no added substrate (N = 15), and b) with oyster shell substrate (N = 27). Letters denote statistically significant differences between treatments based on Tukey’s HSD test. Error bars represent 1 S.E. doi:10.1371/journal.pone.0079337.g008

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Lillis, A., Eggleston, D. B., & Bohnenstiehl, D. R. (2013). Oyster larvae settle in response to habitat-associated underwater sounds. PLoS ONE, 8(10). https://doi.org/10.1371/journal.pone.0079337

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