Soundscape analysis can be an effective tool in assessing seagrass restoration early success.
Posidonia oceanica
Acoustic restoration
Fish sound
Mediterranean sea
Passive acoustic monitoring
Restoration success
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
08 Sep 2024
08 Sep 2024
Historique:
received:
26
03
2024
accepted:
02
09
2024
medline:
9
9
2024
pubmed:
9
9
2024
entrez:
8
9
2024
Statut:
epublish
Résumé
Restoration of vulnerable marine habitats is becoming increasingly popular to cope with widespread habitat loss and the resulting decline in biodiversity and ecosystem services. Lately, restoration strategies have been employed to enhance the recovery of degraded meadows of the Mediterranean endemic seagrass Posidonia oceanica. Typically, habitat restoration success is evaluated by the persistence of foundation species after transplantation (e.g., plant survival and growth) on the short and long-term, although successful plant responses do not necessarily reflect the recovery of ecosystem biodiversity and functions. Recently, soundscape (the spatial, temporal and frequency attribute of ambient sound and types of sound sources characterizing it) has been related to different habitat conditions and community structures. Thus, a successful restoration action should lead to acoustic restoration and soundscape ecology could represent an important component of restoration monitoring, leading to assess successful habitat and community restoration. Here, we evaluated acoustic community and metrics in a P. oceanica restored meadow and tested whether the plant transplant effectiveness after one year was accompanied by a restored soundscape. With this goal, acoustic recordings from degraded, transplanted and reference meadows were collected in Sardinia (Italy) using passive acoustic monitoring devices. Soundscape at each meadow type was examined using both spectral analysis and classification of fish calls based on a catalogue of fish sounds from the Mediterranean Sea. Seven different fish sounds were recorded: most of them were present in the reference and transplanted meadows and were associated to Sciaena umbra and Scorpaena spp. Sound Pressure Level (SPL, in dB re: 1 μPa-rms) and Acoustic Complexity Index (ACI) were influenced by the meadow type. Particularly higher values were associated to the transplanted meadow. SPL and ACI calculated in the 200-2000 Hz frequency band were also related to high abundance of fish sounds (chorus). These results showed that meadow restoration may lead to the recovery of soundscape and the associated community, suggesting that short term acoustic monitoring can provide complementary information to evaluate seagrass restoration success.
Identifiants
pubmed: 39245725
doi: 10.1038/s41598-024-71975-2
pii: 10.1038/s41598-024-71975-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
20910Informations de copyright
© 2024. The Author(s).
Références
Adams, S. M. Assessing cause and effect of multiple stressors on marine systems. Mar. Pollut. Bull. 51, 649–657 (2005).
pubmed: 16291182
doi: 10.1016/j.marpolbul.2004.11.040
Costanza, R. R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997).
doi: 10.1038/387253a0
Kennish, M. J. Management strategies to mitigate anthropogenic impacts in estuarine and coastal marine environments: A review. Open J. Ecol. 12, 667–688 (2022).
doi: 10.4236/oje.2022.1210038
Heck, K. L., Hays, G. & Orth, R. J. Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar. Ecol. Progr. Ser. 253, 123–136 (2003).
doi: 10.3354/meps253123
Macreadie, P. I., Baird, M. E., Trevathan-Tackett, S. M., Larkum, A. W. & Ralph, P. J. Quantifying and modelling the carbon sequestration capacity of seagrass meadows—A critical assessment. Mar. Pollut. Bull. 83, 430–439 (2014).
pubmed: 23948090
doi: 10.1016/j.marpolbul.2013.07.038
McLeod, E. et al. A blueprint for blue carbon: Toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front. Ecol. Environ. 9, 552–560 (2011).
doi: 10.1890/110004
Gattuso, J. P., Magnan, A. K., Bopp, L., Cheung, W. W., Duarte, C. M., Hinkel, J., et al. Ocean solutions to address climate change and its effects on marine ecosystems. Front. Mar. Sci. 337 (2018).
Hemminga, M. A., Duarte, C. M. Seagrass Ecology (Cambridge University Press, 2000). https://doi.org/10.1017/cbo9780511525551 .
Larkum, A. W. D., Orth, R. J. & Duarte, C. M. Seagrasses: Biology, ecology and conservation. Phycologia 45, 5 (2006).
Fonseca, M. S., Kenworthy, W. J., Thayer, G. W. Guidelines for the Conservation and Restoration of Seagrasses in the United States and Adjacent Waters (Science for Solutions, 1998).
Lamb, J. B., van de water, J. A. J. M., Bourne, D. G., Hein, M. Y., Fiorenza, E. A., et al. Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355, 731–733 (2017).
Jayathilake, D. R. M. & Costello, M. J. A. Modelled global distribution of the seagrass biome. Biol. Conserv. 226, 120–126 (2018).
doi: 10.1016/j.biocon.2018.07.009
Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. 106, 12377–12381 (2009).
pubmed: 19587236
pmcid: 2707273
doi: 10.1073/pnas.0905620106
Dunic, J. C., Brown, C. J., Connolly, R. M., Turschwell, M. P. & Côté, I. M. Long-term declines and recovery of meadow area across the world’s seagrass bioregions. Glob. Change Biol. 27, 4096–4109 (2021).
doi: 10.1111/gcb.15684
Marbà, N., Díaz-Almela, E. & Duarte, C. M. Mediterranean seagrass (Posidonia oceanica) loss between 1842 and 2009. Biol. Conserv. 176, 183–190 (2009).
doi: 10.1016/j.biocon.2014.05.024
Orth, R. J. et al. A global crisis for seagrass ecosystems. Bioscience 56, 987–996 (2006).
doi: 10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2
Perkol-Finkel, S. & Airoldi, L. Loss and recovery potential of marine habitats: an experimental study of factors maintaining resilience in subtidal algal forests at the Adriatic Sea. PLoS One 5, e10791 (2010).
pubmed: 20520726
pmcid: 2875393
doi: 10.1371/journal.pone.0010791
Carr, J., D’Odorico, P., McGlathery, K. & Wiberg, P. Stability and bistability of seagrass ecosystems in shallow coastal lagoons: Role of feedbacks with sediment resuspension and light attenuation. J. Geophys. Res. 115, G03011 (2010).
McGlathery, K. J. et al. Nonlinear dynamics and alternative stable states in shallow coastal systems. Oceanography 26, 220–231 (2013).
doi: 10.5670/oceanog.2013.66
Fonseca, M. S., Julius, B. E. & Kenworthy, W. J. Integrating biology and economics in seagrass restoration: How much is enough and why?. Ecol. Eng. 15, 227–237 (2000).
doi: 10.1016/S0925-8574(00)00078-1
van Katwijk, M. M. et al. Global analysis of seagrass restoration: The importance of large-scale planting. J. Appl. Ecol. 53, 567–578 (2016).
doi: 10.1111/1365-2664.12562
SER (Society for Ecological Restoration International Science & Policy Working Group). The SER Primer on Ecological Restoration. (Society for Ecological Restoration, Science & Policy Working Group, 1998).
SER (Society for Ecological Restoration International Science & Policy Working Group). The SER International Primer on Ecological Restoration (available from www.ser.org ). (Society for Ecological Restoration International, 2004).
Bullock, J. M., Aronson, J., Newton, A. C., Pywell, R. F. & Rey-Benayas, J. M. Restoration of ecosystem services and biodiversity: Conflicts and opportunities. Trends Ecol. Evol. 26, 541–549 (2011).
pubmed: 21782273
doi: 10.1016/j.tree.2011.06.011
Peterson, C. H., Kneib, R. T. & Manen, C. A. Scaling restoration actions in the marine environment to meet quantitative targets of enhanced ecosystem services. Mar. Ecol. Progr. Ser. 264, 73–176 (2003).
doi: 10.3354/meps264173
Shackelford, N. et al. Primed for change: Developing ecological restoration for the 21st century. Restor. Ecol. 21, 297–304 (2013).
doi: 10.1111/rec.12012
Valdez, S. R. et al. Positive ecological interactions and the success of seagrass restoration. Front. Mar. Sci. 7, 91 (2020).
doi: 10.3389/fmars.2020.00091
Fournet, M. E. H., Stabenau, E., Madhusudhana, S. & Rice, A. N. Altered acoustic community structure indicates delayed recovery following ecosystem perturbations. Estuarine Coast. Shelf Sci. 274, 107948 (2022).
doi: 10.1016/j.ecss.2022.107948
Tan, Y. M. et al. Seagrass restoration is possible: Insights and lessons from Australia and New Zealand. Front. Mar. Sci. 7, 1–21 (2020).
doi: 10.3389/fmars.2020.00617
Boudouresque, C. F., Blanfuné, A., Pergent, G. & Thibaut, T. Restoration of seagrass meadows in the Mediterranean Sea: A critical review of effectiveness and ethical issues. Water 13, 1034 (2021).
doi: 10.3390/w13081034
Pansini, A., Bosch-Belmar, M., Berlino, M., Sarà, G. & Ceccherelli, G. Collating evidence on the restoration efforts of the seagrass Posidonia oceanica: Current knowledge and gaps. Sci. Total Environ. 851, 158320 (2022).
pubmed: 36037894
doi: 10.1016/j.scitotenv.2022.158320
Bacci, T., La Porta, B., Maggi, C., Nonnis, O., Paganelli, D., Rende, F.S., Targusi, M. Conservazione e Gestione Della Naturalità Negli Ecosistemi Marino-Costieri. In Il Trapianto Delle Praterie di Posidonia oceanica. Manuali e Linee Guida n.106/2014; ISPRA: Rome, Italy, 2014, 1–97 (2014).
Noss, R. F. Indicators for monitoring biodiversity: A hierarchical approach. Conserv. Biol. 4, 355–364 (1990).
doi: 10.1111/j.1523-1739.1990.tb00309.x
Ruiz-Jaen, M. C. & Aide, T. M. Restoration success: How is it being measured?. Restor. Ecol. 13, 569–577 (2005).
doi: 10.1111/j.1526-100X.2005.00072.x
Ruiz-Jaen, M. C. & Aide, T. M. Vegetation structure, species diversity, and ecosystem processes as measures of restoration success. For. Ecol. Manag. 218, 159–173 (2005).
doi: 10.1016/j.foreco.2005.07.008
Scapin, L., Zucchetta, M., Facca, C., Sfriso, A. & Franzoi, P. Using fish assemblage to identify success criteria for seagrass habitat restoration. Web Ecol. 16, 33–36 (2016).
doi: 10.5194/we-16-33-2016
Beheshti, K.M., Williams, S.L., Boyer, K.E., Endris, C., Clemons, A., Grimes, T. et al. Rapid enhancement of multiple ecosystem services following the restoration of a coastal foundation species. Ecol. Appl. 32, e02466 (2022).
Murphy, H. M. & Jenkins, G. P. Observational methods used in marine spatial monitoring of fishes and associated habitats: A review. Mar. Freshw. Res. 61, 236–252 (2010).
doi: 10.1071/MF09068
Staaterman, E. et al. Bioacoustic measurements complement visual biodiversity surveys: Preliminary evidence from four shallow marine habitats. Mar. Ecol. Progr. Ser. 575, 207–215 (2017).
doi: 10.3354/meps12188
Pijanowski, B. C. et al. Soundscape ecology: The science of sound in the landscape. BioScience 61, 203–216 (2011).
doi: 10.1525/bio.2011.61.3.6
Sueur, J., Aubin, T. & Simonis, C. Seewave: A free modular tool for sound analysis and synthesis. Bioacoustics 18, 213–226 (2008).
doi: 10.1080/09524622.2008.9753600
Butler, J., Stanley, J. A. & Butler, M. J. Underwater soundscapes in near-shore tropical habitats and the effects of environmental degradation and habitat restoration. J. Exp. Mar. Biol. Ecol. 479, 89–96 (2016).
doi: 10.1016/j.jembe.2016.03.006
Rossi, T., Connell, S. D. & Nagelkerken, I. The sounds of silence: Regime shifts impoverish marine soundscapes. Landsc. Ecol. 32, 239–248 (2017).
doi: 10.1007/s10980-016-0439-x
Gordon, T. A. et al. Acoustic enrichment can enhance fish community development on degraded coral reef habitat. Nat. Commun. 10, 1–7 (2019).
doi: 10.1038/s41467-019-13186-2
Angelini, C. et al. Foundation species’ overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes. Proc. R. Soc. B 282, 1–9 (2015).
doi: 10.1098/rspb.2015.0421
Toma, T. S. P., Overbeck, G. E., de Mendonça, M. S., Fernandes, G. W. Optimal references for ecological restoration: The need to protect references in the tropics. Perspect. Ecol. Conserv. 21, 25–32 (2023).
Stewart, B. D. & Beukers, J. S. Baited technique improves censuses of cryptic fish in complex habitats. Mar. Ecol. Progr. Ser. 197, 259–272 (2000).
doi: 10.3354/meps197259
Di Iorio, L. et al. Posidonia meadows calling: A ubiquitous fish sound with monitoring potential. Remote Sens. Ecol. Conserv. 4, 248–263 (2018).
doi: 10.1002/rse2.72
Bolgan, M., Di Iorio, L., Dailianis, T., Catalan, I.A., Lejeune, P., Picciulin, M. et al. Fish acoustic community structure in Neptune seagrass meadows across the Mediterranean basin. Aquat. Conserv. Mar. Freshw. Ecosyst. 1–19 (2022).
La Manna, G. et al. Marine soundscape and fish biophony of a Mediterranean marine protected area. PeerJ 9, e12551 (2021).
pubmed: 35003918
pmcid: 8684326
doi: 10.7717/peerj.12551
Picciulin, M., Calcagno, G., Sebastianutto, L., Bonacito, C., Codarin, A., Costantini, M. et al. Diagnostics of nocturnal calls of Sciaena umbra (L., fam., Sciaenidae) in a nearshore Mediterranean marine reserve. Bioacoustics. 22, 3 (2012).
Froese, R., Pauly, D. Editors. 2024.FishBase. World Wide Web electronic publication. www.fishbase.org (2024).
Lillis, A., Eggleston, D. B. & Bohnenstiehl, D. R. Estuarine soundscapes: Distinct acoustic characteristics of oyster reefs compared to soft-bottom habitats. Mar. Ecol. Progr. Ser. 505, 1–17 (2014).
doi: 10.3354/meps10805
Borg, J. A. et al. Wanted dead or alive: High diversity of macroinvertebrates associated with living and ‘dead’ Posidonia oceanica matte. Mar. Biol. 149, 667–677 (2006).
doi: 10.1007/s00227-006-0250-3
Coquereau, L. et al. Sound production and associated behaviours of benthic invertebrates from a coastal habitat in the north-east Atlantic. Mar. Biol. 163, 127 (2016).
doi: 10.1007/s00227-016-2902-2
Ceccherelli, G., Pais, A., Pinna, S., Serra, S. & Sechi, N. On the movement of the sea urchin Paracentrotus lividus towards Posidonia oceanica seagrass patches. J. Shellfish Res. 28, 397–403 (2009).
doi: 10.2983/035.028.0224
Radford, C. A., Stanley, J. A., Simpson, S. D. & Jeffs, A. G. Juvenile coral reef fish use sound to locate habitats. Coral Reefs 30, 295–305 (2011).
doi: 10.1007/s00338-010-0710-6
Piercy, J. J. B., Codling, E. A., Hill, A. J., Smith, D. J. & Simpson, S. D. Habitat quality affects sound production and likely distance of detection on coral reefs. Mar. Ecol. Progr. Ser. 516, 35–47 (2014).
doi: 10.3354/meps10986
Freeman, L. A. & Freeman, S. E. Rapidly obtained ecosystem indicators from coral reef soundscapes. Mar. Ecol. Progr. Ser. 561, 69–82 (2016).
doi: 10.3354/meps11938
Ricci, S. W., Eggleston, D. B., Bohnenstiehl, D. R. & Lillis, A. Temporal soundscape patterns and processes in an estuarine reserve. Mar. Ecol. Progr. Ser. 550, 25–38 (2016).
doi: 10.3354/meps11724
Elise, S. et al. Assessing key ecosystem functions through soundscapes: A new perspective from coral reefs. Ecol. Indic. 107, 105623 (2019).
doi: 10.1016/j.ecolind.2019.105623
Hughes, S. J., Ellis, D. D., Chapman, D. M. & Staal, P. R. Low-frequency acoustic propagation loss in shallow water over hard-rock seabeds covered by a thin layer of elastic–solid sediment. J. Acoust. Soc. Am. 88, 283–297 (1990).
doi: 10.1121/1.399951
Buscaino, G. et al. Temporal patterns in the soundscape of the shallow waters of a Mediterranean marine protected area. Sci. Rep. 6, 34230 (2016).
pubmed: 27677956
pmcid: 5039702
doi: 10.1038/srep34230
Dimoff, S. A. et al. The utility of different acoustic indicators to describe biological sounds of a coral reef soundscape. Ecol. Indic. 124, 107435 (2021).
doi: 10.1016/j.ecolind.2021.107435
Harris, S. A., Shears, N. T. & Radford, C. A. Ecoacoustic indices as proxies for biodiversity on temperate reefs. Methods Ecol. Evol. 7, 713–724 (2016).
doi: 10.1111/2041-210X.12527
Nguyen Hong Duc, P. Cazau, D., White, P.R., Gérard, O., Detcheverry, J., Urtizberea, F., Adam, O. Use of ecoacoustics to characterize the marine acoustic environment off the North Atlantic French Saint-Pierre-et-Miquelon Archipelago. J. Mar. Sci. Eng. 9, 177 (2021).
Pieretti, N., Farina, A. & Morri, D. A new methodology to infer the singing activity of an avian community: The Acoustic Complexity Index (ACI). Ecol. Indic. 11, 868–873 (2011).
doi: 10.1016/j.ecolind.2010.11.005
Alcocer, I., Lima, H., Sugai, L. S. M. & Llusia, D. Acoustic indices as proxies for biodiversity: A meta-analysis. Biol. Rev. 97, 2209–2236 (2022).
pubmed: 35978471
doi: 10.1111/brv.12890
Bolgan, M. et al. Acoustic Complexity of vocal fish communities: A field and controlled validation. Sci. Rep. 8, 10559 (2018).
pubmed: 30002420
pmcid: 6043554
doi: 10.1038/s41598-018-28771-6
Pansini, A., Deroma, M., Guala, I., Monnier, B., Pergent-Martini, C., Piazzi, L., et al. The resilience of transplanted seagrass traits encourages detection of restoration success. J. Environ. Manag. 357 (2024).
Bertucci, F., Lejeune, P., Payrot, J. & Parmentier, E. Sound production by dusky grouper Epinephelus marginatus at spawning aggregation sites. J. Fish Biol. 87, 400–421 (2015).
pubmed: 26177857
doi: 10.1111/jfb.12733
Kaplan, M., Mooney, T., Partan, J. & Solow, A. Coral reef species assemblages are associated with ambient soundscapes. Mar. Ecol. Progr. Ser. 533, 93–107 (2015).
doi: 10.3354/meps11382
Buia, M. C., Gambi, M. C. & Dappiano, M. The seagrass systems. Biol. Mar. Mediterranea 11, 133–184 (2004).
La Porta, B., Bacci, T. Manual for the Planning, Implementation and Monitoring of Transplantation of Posidonia oceanica (ed. La Porta, B.) (Bacci Tiziano Italian Institute for Environmental Protection and Research-ISPRA, 2022).
Kéver, L., Lejeune, P., Michel, L. N. & Parmentier, E. Passive acoustic recording of Ophidion rochei calling activity in Calvi Bay (France). Mar. Ecol. 37, 1315–1324 (2016).
doi: 10.1111/maec.12341
Desiderà, E. et al. Acoustic fish communities: Sound diversity of rocky habitats reflects fish species diversity. Mar. Ecol. Progr. Ser. 608, 183–197 (2019).
doi: 10.3354/meps12812
Cato, D. H. Marine biological choruses observed in tropical waters near Australia. J. Acoust. Soc. Am. 64, 736–743 (1978).
doi: 10.1121/1.382038
Bradfer-Lawrence, T., Desjonqueres, C., Eldridge, A., Johnston, A., Metcalf, O. Using acoustic indices in ecology: Guidance on study design, analyses and interpretation. Methods Ecol. Evol. 00, 1–13 (2022).
R Core Team. R: A Language and Environment for Statistical Computing (2019).
Merchant, N. D. et al. Measuring acoustic habitats. Methods Ecol. Evol. 6, 257–265 (2015).
pubmed: 25954500
pmcid: 4413749
doi: 10.1111/2041-210X.12330
Villanueva-Rivera, L.J., Pijanowski, B.C. Soundscape Ecology, R package version 1.3.3. https://CRAN.R-project.org/package=soundecology (2018).
Lindseth, A. & Lobel, P. Underwater soundscape monitoring and fish bioacoustics: A review. Fishes 3, 36 (2018).
doi: 10.3390/fishes3030036
McWilliam, J. N. & Hawkins, A. D. A comparison of inshore marine soundscapes. J. Exp. Mar. Biol. Ecol. 446, 166–176 (2013).
doi: 10.1016/j.jembe.2013.05.012
Archer, S. et al. First description of a glass sponge reef soundscape reveals fish calls and elevated sound pressure levels. Mar. Ecol. Progr. Ser. 595, 245–252 (2018).
doi: 10.3354/meps12572
Brooks, M. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
doi: 10.32614/RJ-2017-066
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., Smith, G.H. Mixed Effects Models and Extensions in Ecology with R 579 (2009).
Pieretti, N. & Danovaro, R. Acoustic indexes for marine biodiversity trends and ecosystem health. Philos. Trans. R. Soc. 375, 2090447 (2020).
doi: 10.1098/rstb.2019.0447