An international team led by researchers from the University of Liège used underwater audio recordings for understanding fish diversity in the Mediterranean Sea. The research team included a MSCA-COFUND postdoctoral fellow (Dr. Marta Bolgan) based in the European leading laboratory in the field of functional morphology of fish sound production mechanisms (MORFONCT; Prof. Eric Parmentier) and a long list of international collaborators. This MSCA COFUND fellowship was called BEIPD, which means “BE an International PostDoc” and the fellow had surely taken this literally; she has travelled all around Europe for collecting her data, proving that international collaborations are the lifeblood of a successful (and joyful) research career.
Oceans have been long assumed to be quiet, as shown by the title of Jacques Cousteau’s 1956 movie “The Silent World”. Nothing but a silent world, oceans are actually filled with numerous sound sources: abiotic sources generate geophonies, sounds emitted by living organisms generate biophonies and man-made noise generates anthrophonies. All together, these sounds form the acoustic environment (soundscape). Each aquatic habitat is characterised by a unique, localised soundscape, where sonic sources may consistently change over relatively short periods and geographical scales [2-4]. Each localised soundscape conveys a complex sonic narrative loaded with critical information for the survival of any sentient animal which inhabits it[5-7].
Many species of fish produce sounds (alone or in chorus) under a variety of conditions, such as when engaging in reproductive activities, defending territory or offspring, competing for food, responding to threats, synchronising mating, calling for conspecifics or as a by-product of their activities (see sound libraries of both MORFONCT and CHORUS) Fish have evolved the largest diversity of sound-generating mechanisms among vertebrates. This in its turns results in a wide diversity of sounds emitted by different species, which features are species-specific in most cases. In other words, we should be able to recognise different fish species only on the basis of their calls, exactly as many naturalists identify birds by listening to their songs. Listening to fish calls, we can achieve information about which species is present in a specific environment and where and when it prefers to aggregate.
Passive acoustic monitoring (PAM) involves the use of hydrophones to receive and record all the components of underwater soundscapes, including fish calls. PAM represents a non-invasive way to assess temporal and spatial patterns of distribution of calling individuals. Several studies used PAM to investigate different aspects of vocal fish populations, such as presence, distribution, relative abundance, diel, lunar and seasonal cycle of activity as well as for delimitating spawning areas and for studying wild fish spawning behaviour [11-21]. Since sound emission is associated with reproduction in many species, this method became especially useful for monitoring spawning sites at both temporal and geographical scales, and is now considered a powerful tool for conservation studies[15-16][22-23]. The knowledge that can be gathered using PAM is indeed of fundamental importance for monitoring vulnerable or commercially important fish species, for determining appropriated fishing periods as well as for informing effective conservation plans, by protecting the animals during their reproductive season. Furthermore, PAM can provide critical information for understanding the impact of human activities on fish populations, such as how anthropogenic activities (fishing, pilling, wind farm, etc) influence fish vocal behaviour, displacement and activities [24-26] or how climate change impacts on biodiversity. Natural sounds collected using PAM, especially those from vocal animals, can be used as proxies to learn about the diversity of species, habitat quality and the phenology of biological events.
The BEIPD fellowship “Sonata for Teleosts: fish sounds as proxies to learn about the diversity of species” aimed to address three work packages:
- Work package 1: SOUNDS CATALOGUE of FISH INHABITING the CALVI BAY (Corsica, France);
- Work package 2: SEASONAL and GEOGRAPHICAL VARIATION OF CALVI SOUNDSCAPE;
- Work package 3: CAPTIVITY RECORDINGS: SPECIES IDENTITY.
Work package 1: Audition of recordings previously collected by MORFONCT included recordings collected at -40 m in sandy habitats in front of STARESO research station (Calvi Bay, Corsica, France). This analysis, which was carried out during the initial phases of the BEIPD, was aimed to catalogue fish sound types and to test recent, commonly applied automated procedures for the analysis of large acoustic datasets. This work resulted in two international peer-reviewed publications; the first describes the fish vocal community at -40 m (July) in sandy habitats of the Calvi Bay and tests the performance of the Acoustic Complexity Index to provide information about fish vocal dynamics .
The second publication was carried out thanks to international collaboration and data sharing. In particular, MORFONCT had previously characterised in details the sound types, the vocal dynamics as well as the morphology of the sound producing apparatus of the cryptic fish species Ophidion rochei [28-32]. A sub-set of O. rochei sounds recorded by MORFONCT was used for comparison with previously collected recordings of Dr. Marta Picciulin in the Trieste Gulf (Italy). This comparison allowed to identify the presence of O. rochei thanks to its calls in the Marine Protected Area of Miramare (Italy), an area in which visual census of the fish fauna has been carried out for decades but the presence of O. rochei has always gone unnoticed . We cannot see it….but we can hear it!
During the BEIPD, new acoustic data have been collected in the Calvi Bay, specifically at -20 m in Posidonia oceanica meadows and at -140 m, at the head of a submarine canyon. This latter dataset was added to that collected at similar depths in different seasons by the Research Institute CHORUS; analysis is now concluded and a manuscript is almost ready for submission. To the best of our knowledge, this represents the first description of potential fish sounds recorded in Mediterranean waters below 100 m depth. Altogether, these studies will soon allow to produce a catalogue of fish sounds recorded in different environments of the Calvi Bay.
Work package 2: Although initial aims were restricted to the Calvi Bay (Corsica, France), the geographical scale of the investigation has been enlarged, focusing on one of the least described Mediterranean vocal fish community, i.e. the one inhabiting the endemic environment of Neptune seagrass (Posidonia oceanica) meadows. In particular, this work will shed light on how different vocal fish species share the same acoustic space. During 3 months of consecutive fieldwork, Dr. Bolgan used a combination of vessel-based Passive Acoustic Monitoring (PAM) and Static Acoustic Monitoring in the Tyrrenian (Calvi, Corsica), Balearic (Mallorca, Spain) and Aegean Sea (Crete, Greece). A true acoustic Odyssey! The underlying hypothesis were; i) the vocal community of P. oceanica is composed of different sound types which shows frequency and temporal partition; ii) some sound types are present along the entire Mediterranean axis, where their sound features variation is related to environmental conditions and taxonomic diversity; iii) some other sound types are present in one site only (“acoustic endemism”); 4) the highest number of acoustic endemisms may be found in Crete, potentially highlighting Lessepsian migrations. Analysis of these recordings is ongoing and it is carried out in collaboration with CHORUS Research Institute. A manuscript will be soon ready for submission.
Work package 3: PAM is dependent on the evidence that sounds recorded in the wild actually belong to a specific species. Evidence for the identity of the species that produces a particular sound is often obtained by comparing the remotely recorded PAM sounds with known sounds recorded either in captivity, or, preferably whenever possible, in the field with in situ methodologies. Furthermore, if a precise relationship between sound characteristics and spawning can be found in specific species, this could greatly contribute to the conservation of these species, as we could be able to locate and to protect their spawning areas thanks to a completely not invasive methodology such as PAM. In this context, three investigations have been carried out;
- Together with a Master student, Miss. Justine Soulard, the identity of the unknown species emitting the most abundant fish sound in Neptune seagrass meadows, (the so-called “Kwa”) has been investigated by using an inter-disciplinary and multi-approach. A publication is almost ready for submission.
- Together with another Master student, Miss. Aurora Crucianelli, the potential of Mediterranean fish sounds to provide information about fish status, readiness to spawn and reproductive success has been investigated in fish species of high commercial value (Sciaenidae spp). This investigation was carried out thanks to data previously collected by MORFONCT and in collaboration with HCMR (Crete). In particular, two Mediterranean Sciaenidae species (Argyrosomous regius and Umbrina cirrosa) are housed at HCMR Crete where breeding is induced and monitored. A publication is envisaged by early 2019.
- MORFONCT has long-term experience in the recording and characterization ofsound production mechanisms in Ophidiiformes. However, sounds recordings and morphological investigations are currently lacking for one Mediterranean species, Parophidion vassalli. During the BEIPD, some specimens of Parophidion vassalli have been recorded in captivity at MORFONCT and morphological examinations will be soon carried out. Furthermore, Passive Acoustic Monitoring has been carried out where these specimens were fished; the hypothesis is that Parophidion vassalli can be located in the wild thanks to the sounds recorded at ULiege. The analysis is ongoing.
In synthesis, many questions have been and are still tackled during “Sonata for teleosts”. The supervisor Prof. Parmentier has provided Dr. Marta Bolgan with the perfect intellectual environment for deepening her knowledge of fish sound production (from mechanisms to diversity) and for expanding her range of skills in Passive Acoustic Monitoring (from coastal to deep waters). During the BEIPD, Dr Marta Bolgan had the possibility of strengthening previous international collaborations and to initiate new ones. International, collaborative scientific networks permit to avoid to replicate results between research groups and allow for a more effective questioning- answering around biological questions, which is the core of biology research. As in nature, everything is connected to everything, and the most diverse environments are the most resilient and productive, so researchers in different field of biology gain amazing benefits by working in collaborative networks and by sharing their knowledge.
Concluding, it has to be considered that the analysis of acoustic datasets is an extremely time-consuming task, and therefore some of the most exciting findings of this BEIPD will be published in the next years. Stay tuned 😀
 Farina A. 2014. Soundscape Ecology: Principles, Patterns, Methods and Applications. New York: USA.
 Krause B.L. 2012. The Great Animal Orchestra (Enhanced): Finding the Origins of Music in the World’s Wild Places. New York: NY.
 Radford C. A., Stanley J. A., Tindle C.T., Montgomery J. C., Jeffs A.G. 2010. Localised coastal habitats have distinct underwater sound signatures. Marine Ecology Progress Series 401: 21-29.
 Staaterman E., Paris C.B., DeFerrari H.A., Mann D.A., Rice A.N., Alessandro E.K. 2014. Celestial patterns in marine soundscapes. Marine Ecology Progress Series 508: 17-32.
 Bertucci F., Parmentier E., Berten L., Brooker R.M., Lecchini D. 2015. Temporal and spatial comparisons of underwater sound signatures of different reef habitats in Moorea Island, French Polynesia. PLoS ONE 10(9): e0135733.
 Pijanowski B.C, Villanueva-Rivera L.J, Dumyahn S.L., Farina A., Krause B.L., Napoletano B.M., Gage S.H., Pieretti N. 2011. Soundscape ecology: the science of sound in the landscape. BioScience 61(3): 203-216.
 Krause B., Farina, A .2016. Using ecoacoustic methods to survey the impacts of climate change on biodiversity. Biological Conservation 195: 245-254.
 Amorim M.C.P. 2006. Communication in fishes. Enfield: NH and Plymouth: UK. Chapter 3, Diversity of sound production in fish, p. 71–105.
 Fine M.L., Parmentier E. 2015. Sound Communication in Fishes. Ladich F (ed.), Springer, Wien. Chapter: Mechanisms of Fish Sound Production In Sound Communication in Fishes, p. 77-126
 Rountree R.A., Gilmore R.G., Goudey C.A., Hawkins A.D., Luczkovich J.J., Mann D. 2006. Listening to fish: application of passive acoustic to fisheries science. Fisheries 31(9): 433-446.
 Fish M.P., Mowbray W.H. 1970. Sounds of Western Atlantic fishes. John Howkings, Baltimore.
 Mann D.A., Lobel P. S. 1995. Passive acoustic detection of sounds produced by the damselfish, Dascyllus albisella (Pomacentridae).Bioacoustics 6(3): 199-213.
 Topping D.T., Lowe C.G., Caselle, J.E. 2006. Site fidelity and seasonal movement patterns of adult California sheephead Semicossyphus pulcher (Labridae): an acoustic monitoring study. Marine Ecology Progress Series 326: 257-267.
 Locascio J.V., Mann D.A. 2008. Diel patterns of fish sound production in Charlotte Harbor, FL. Transaction of the American Fishery Society 137:606-615.
 Luczkovich J.J., Pullinger R.C., Johnson S.E. 2008. Identifying sciaenid critical spawning habitats by the use of passive acoustics. Transactions of the American Fishery Society 137: 576–605.
 Fine M.L., Thorson R.F. 2008. Use of Passive Acoustics for Assessing Behavioral Interactions in Individual Toadfish. Transaction of the American Fishery Society 137:627-637.
 Gannon D.P., Gannon J.G. 2009. Assessing trends in the density of Atlantic croaker (Micropogonias undulatus): a comparison of passive acoustic and trawl methods. Fishery Bulletin 108(1): 106-116.
 Hernandez K.M., Risch D., Cholewiak D.M., Dean M. J., Hatch L.T., Hoffman W. S, Rice A.N., Zemeckis D., Van Parijs S. M. 2013. Acoustic monitoring of Atlantic cod (Gadus morhua) in Massachusetts Bay: implications for management and conservation. ICES Journal of Marine Science: Journal du Conseil, fst003.
 Picciulin M., Bolgan M., Codarin A., Fiorin R., Zucchetta M., Malavasi S. 2013a. Passive acoustic monitoring of Sciaena umbra on rocky habitats in the Venetian littoral zone. Fishery Research. 145: 76-81.
 Picciulin M., Calcagno G., Sebastianutto L., Bonacito C., Codarin A., Costantini M., Ferrero E.A. 2013b. Diagnostics of nocturnal calls of Sciaena umbra (L., fam. Sciaenidae) in a nearshore Mediterranean marine reserve. Bioacoustics 22(2): 109-120.
 Wall C.C., Simard P., Lembke C., Mann D.A. 2013. Large-scale passive acoustic monitoring of fish sound production on the West Florida Shelf. Marine Ecology Progress Series 484: 173-188.
 Gannon D.P. 2008. Passive Acoustic Techniques in Fisheries Science: A Review and Prospectus. Transactions of the American Fishery Society 137:638-656.
 Luczkovich J.J., Sprague M.W., Johnson S.E., Pullinger R.C. 1999. Delimiting spawning areas of weakfish, Cynoscion regalis (family Sciaenidae) in Pamlico Sound, North Carolina using passive hydroacoustic surveys. Bioacoustics 10:143-160.
 Hastings M.C., Popper A.N. 2005. Effects of Sound on Fish. California Department of Transportation Con-tract 43A0139, Task Order 1.
 Popper A.N., Hastings M.C. 2009a. Effects of anthropogenic sources of sound on fishes. Journal of Fish Biology 75:455-489.
 Popper A.N., Hastings M.C. 2009b. The effects on fish of human-generated (anthropogenic) sound. Integrative Zoology 4:43-52.
 Bolgan M., Amorim M.C.P., Fonseca P.J., Di Iorio L. & Parmentier E. (2018). Acoustic Complexity of vocal fish communities: a field and control validation. Scientific reports, 8(1): 10559.
 Parmentier, E., Bouillac, G., Dragicevic, B., Dulcic, J., Fine, M. L., Dragičević, B., … Fine, M. L. (2010). Call properties and morphology of the sound-producing organ in Ophidion rochei (Ophidiidae). Journal of Experimental Biology, 213, 3230–3236.
 Kéver, L., Boyle, K. S., Dragičević, B., Dulčić, J., Casadevall, M., & Parmentier, E. (2012). Sexual dimorphism of sonic apparatus and extreme intersexual variation of sounds in Ophidion rochei (Ophidiidae): first evidence of a tight relationship between morphology and sound characteristics in Ophidiidae. Frontiers in Zoology, 9, 1–16.
 Kéver, L., Boyle, K. S., Bolen, G., Dragičević, B., Dulčić, J., & Parmentier, E. (2014). Modifications in call characteristics and sonic apparatus morphology during puberty in Ophidion rochei (Actinopterygii: Ophidiidae). Journal of Morphology, 275, 650–660.
 Kéver, L., Boyle, K. S., & Parmentier, E. (2015). Effects of seawater temperature on sound characteristics in Ophidion rochei (Ophidiidae). Journal of Fish Biology, 87(2), 502–509.
 Kéver, L., Lejeune, P., Michel, L. N., & Parmentier, E. (2016). Passive acoustic recording of Ophidion rochei calling activity in Calvi Bay (France). Marine Ecology, 37, 1315–1324.
 Picciulin M., Kever L, Parmentier E., Bolgan M. (in press) Listening to the unseen: Passive Acoustic Monitoring reveals the presence of a cryptic fish species. Aquatic Conservation: Marine and Freshwater Ecosystems.