Boat-induced pressure does not influence breeding site selection of a vulnerable fish species in a highly anthropized coastal area

https://doi.org/10.1016/j.marpolbul.2022.113750Get rights and content

Highlights

  • Sciaena umbra is a vulnerable sonic fish species known to be affected by boat noise

  • S. umbra chorus is a proxy of its spawning activity

  • Chrousing is expected after sunset in deeper calm waters of the Venice inlets

  • Boat abundance and underwater noise levels do not affect the chorusing occurrence

  • The breeding site choice in the inlets is not influences by boat-induced pressure

Abstract

The brown meagre (Sciaena umbra) is a vulnerable vocal fish species that may be affected by boat noise. The breeding site distribution along the anthropized Venice sea inlets was investigated, by using the species' chorusing activity as a proxy of spawning. Passive acoustic campaigns were repeated at 40 listening points distributed within the three inlets during three-time windows in both summer 2019 and 2020. The role of temporal, morphological, and hydrodynamic variables explaining the observed distribution patterns was evaluated using a GLM approach, considering also human-induced pressures among the candidate predictors. The GLM analysis indicates a higher probability of recording S. umbra chorus after sunset in deeper areas of the inlets, characterized by low water current, while the underwater noise overlapping the species' hearing range and boat abundance did not play any role. This suggests that the species' breeding site choice in the inlets was not influences by boat-induced pressure.

Introduction

Coastal underwater habitats are ecologically dynamic and productive areas used by fish larvae, juveniles and adults for reproduction, foraging and shelter (Elliott and Hemingway, 2002). Here the development of fish populations and communities depends on a mix of external drivers, species interactions and internal population processes (Shelton and Mangel, 2011). The main natural factors influencing the occurrence of fishes in coastal ecosystems are habitats and seasons (Franco et al., 2006a; Hajisamae et al., 2006). Habitat features such as depth, current, substratum type, presence of shelter or habitat diversity may play a major role in shaping fish population in space (i.e. Kutti et al., 2015; Scapin et al., 2018a; Wong et al., 2018), whereas precipitation, flow and tidal energy, water temperature and salinity are the main physical parameters structuring fish population in time (Franco et al., 2006b; MacRae and Cowan, 2010). A strong interaction between these components is found in coastal and transitional water bodies, where the spatial gradients are subjected to strong temporal dynamics (Newton et al., 2014; Zucchetta et al., 2016). However, human activities have dramatically altered both abiotic and biotic properties of coastal ecosystems at an alarming rate (Halpern et al., 2008). Urbanization, fisheries, aquaculture, boat traffic, water degradation and sedimentation led to simplified biological assemblages in both structure and function, decreasing in density, richness and diversity and shifting toward populations of few proliferating species (Claudet and Fraschetti, 2010; Lotze et al., 2006). Emerging anthropogenic stressors include microplastics, alien invasive species and increasing water temperature and acidification (Brander, 2013; Katsanevakis et al., 2014; McCormick et al., 2020). The role of anthropogenic pressures in influencing the status and distribution of nekton assemblages has been shown for several coastal ecosystems (e.g. Bergström et al., 2013, Bergström et al., 2016; Cavraro et al., 2019; Östman et al., 2017; Zucchetta et al., 2016, Zucchetta et al., 2021), despite the difficulty of disentangling between the human-induced and the natural variability, typically very high in these types of ecosystems (Elliott and Quintino, 2007).

Anthropogenic underwater noise is another pressure that started gaining the attention of the scientific community (Popper and Hastings, 2009; Rako-Gospić and Picciulin, 2019). In aquatic ecosystems, noise is intentionally produced for seismic exploration or sonar and it is an by-product of industry, shipping, and recreational boating. Coastal-marine soundscapes are rapidly changing and human-generated noise is now a persistent feature of coastal environments and open ocean (Andrew et al., 2002; Duarte et al., 2021; Hildebrand, 2009). Existing evidence shows that anthrophony negatively affects marine animals at multiple levels, including their behaviour, physiology, and survival (extensively review by Di Franco et al., 2020; Duarte et al., 2021; Kunc et al., 2016). As a result, underwater noise has now become a recognized source of pollution in national and international legislations, including the United Nations Convention on the Law of the Sea (UNCLOS; ICP-19, https://undocs.org/A/73/124) and the European Marine Strategy Framework Directive 2008/56/EC (MSFD; EU, 2008).

Although vessel noise is prominent in many ocean regions (Duarte et al., 2021), in coastal areas small boat noises are far more populous and span a wider range of frequencies, with tonal components observed up to 5 kHz, contrasting with the typically narrowband low frequency sound of large ships (Erbe et al., 2012). Within the Inner Danish coastal waters, mid-to-high frequency noise from small recreational vessels have been shown to significantly contribute to the local soundscapes, due to the high densities and close proximities at which they transit this region (Hermannsen et al., 2019). Similarly, a significant increases in the low-frequency component of the soundscape has been highlighted for shallow coastal habitats in New Zealand (Wilson et al., 2022), with boat sound being an omnipresent source of anthrophony, especially in the summer period.

Small boat noise may have potential negative effects on marine species that depend on these habitats to forage, breed and/or rest; these effects include hearing threshold shifts and masking of communication in fishes, stress-related physiological responses and behavioural modification (Slabbekoorn et al., 2010). At the behavioural level, boat noise exposure causes alteration of the schooling behaviour, reduction in territorial defence and decrease in feeding frequency, corresponding to changes of physiological conditions; further exposure to boat noise is also related to a reduction in the spawning activity of fish species and a decrease of the anti-predator response, enhancing in its turn the individual predation risk (reviewed by Di Franco et al., 2020). Ivanova et al. (2020) report a horizontal displacement of Artic cod (Boreogadus saida) from the core area of their home range for periods of vessel presence toward areas with lower noise levels.

In the Mediterranean Sea, in-situ evaluation of boat noise impact has been mostly performed in marine protected areas (MPAs), whose mandate involves separating species from threatening processes; these studies demonstrate short term behavioural changes in fish swimming, feeding, reproductive and territorial activities (Picciulin et al., 2010; Bracciali et al., 2012; La Manna et al., 2016). On the other end of the spectrum there are locations that are intrinsically noisy as ports or inlets, that represent interesting sites to investigate animal responses to underwater noise continuous stressors.

Here we aimed to test the site selection of a vulnerable fish species along a highly anthropized area as the Venice inlets, by using the species' vocal activity for its detection.

The target species of the present study is the brown meagre (Sciaena umbra), a demersal sciaenid fish recognized as indicative of good environmental quality (Garcia-Rubies et al., 2013) and defined as an umbrella species for the ecological community of rocky coastal habitats (Picciulin et al., 2013). Due to overfishing, S. umbra is classified as a vulnerable fish species by the International Union for Conservation of Nature (IUCN). Improvement in the knowledge of this little-known species is required to enhance protection measures, including factors influencing the species habitat and spawning-site selection. Given these consideration, S. umbra is a key species for assessing the risks associated with man-made underwater sound (sensu Hawkins and Popper, 2016), being recognized of conservation interest by legislation, being ecologically relevant and especially vulnerable to noise exposure (Codarin et al., 2009; La Manna et al., 2016; Picciulin et al., 2012b), as it is a vocal fish species. As other Sciaenids, the brown meagre emits drumming sounds during the reproductive period (Codarin et al., 2009; Picciulin et al., 2012a). From the methodological point of view, this also means that the species sounds can be used to identify, map and monitor its functional habitats by passive acoustic monitoring (PAM) technique, in accord to previous studies (Bonacito et al., 2002; Di Iorio et al., 2020; Picciulin et al., 2013); PAM could be applied in areas where visual-based methods are not applicable, as it is the case of the Venice inlets due to the risks connected with high boating and cargo traffic.

By using PAM, the presence of species of conservation and commercial interests as S. umbra, but also as the shi drum Umbrina cirrosa (fam. Sciaenidae), was previously observed along the tidal Venice inlets (Picciulin et al., 2020, Picciulin et al., 2021a, Picciulin et al., 2021b). Here S. umbra was engaged in chorusing activity, which has been proved to be a reliable natural indicator of the species' breeding sites (Picciulin et al., 2020). Interestingly, only the busiest locations in the internal side of the inlets were characterized by chorusing (Picciulin et al., 2021a). Theoretically there were plenty of other suitable sites for the target fish where noise disturbance was minimal, such as the locations facing the open sea; nevertheless, these sites were less exploited by the species. The resulting hypothesis is that other factors than underwater noise, as water current, water depth, bottom structure, and so on, could be crucial for the brown meagre, “forcing” it to remain in some areas regardless of whether or not noise represents a disturbance. In order to evaluate if this is the case, this paper aims to (i) describe the main environmental characteristics of the Venice inlets, (ii) evaluate the S. umbra vocalization distributions over two-season data with special reference to the chorusing activity, (iii) explain this distribution by taking into account the previously considered features of the study area, (iv) focusing in particular on the role of the underwater noise pressure on the S. umbra breeding site selection.

Section snippets

The study area

The Venice Lagoon, one of the largest Mediterranean lagoons, is located in the northern part of the Adriatic Sea (45.2–45.6 N, 12.2–12.6E), within the most industrialized sea areas of the Mediterranean Sea (Menegon et al., 2018), characterized by a traffic of cargos and cruise passengers as well as fishing vessels. All the vessel traffic is forced to pass through the three wide and deep inlets, that allow the navigation from the lagoon to the Adriatic Sea and viceversa, including a conspicuous

Listening point variability for the environmental factors

Patterns in the environmental characteristics of the listening points located in the Venice inlets are highlighted by the Principal Component Analysis (PCA) (Fig. 2), with the first three axes of PCA explaining about 55.57% of the cumulative variance. Some of the variables were highly correlated (Pearson r > 0.7; see Supplementary Fig. S.1), and hence only one variable for each group of correlated variables were retained for the GLM analysis, albeit all of them were included in the PCA (Fig. 2).

Discussion

Over two reproductive seasons, the distribution of S. umbra in the highly anthropized Venice inlets was found to be consistently not random, showing the existence of hot-spots for the species' chorusing, here considered as a proxy of the species spawning activity (Picciulin et al., 2020). The present paper shows that temporal factors as well as morphological, hydrodynamic and local spatial characteristics significantly affected S. umbra vocal activity and therefore its spawning site selection,

Conclusions

In the fields of fishery management and environmental conservation policy, evaluating the effect of human activities on vulnerable populations is of particular interest. This study clearly shows that inferences from evidences of short-term effects should be carefully considered before being extrapolated at wider spatial and temporal scales and to real conditions. S. umbra breeding site choice in the present study appears unaffected by boat-induced pressure, despite multiple evidences of its

CRediT authorship contribution statement

Marta Picciulin: Conceptualization, Methodology, Investigation, Data curation, Formal analysis, Writing – original draft, Writing – review & editing. Matteo Zucchetta: Methodology, Data curation, Formal analysis, Software, Supervision, Visualization, Writing – review & editing. Chiara Facca: Methodology, Project administration, Writing – review & editing. Stefano Malavasi: Conceptualization, Methodology, Funding acquisition, Supervision, Writing – review & editing.

Declaration of Competing Interest

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Marta Picciulin reports financial support was provided by Research Programme Venezia2021, coordinated by CORILA, with the contribution of the Provveditorato for the Public Works of Veneto, Trentino Alto Adige and Friuli Venezia Giulia.

Acknowledgments

Scientific activity was performed in the Research Programme Venezia2021, coordinated by CORILA, with the contribution of the Provveditorato for the Public Works of Veneto, Trentino Alto Adige and Friuli Venezia Giulia. We are grateful to dr. Elisa Coraci and dr. Franco Crosato (Institute for Environmental Protection and Research, ISPRA, Venice) for providing tide level values for the Venice inlets used in the present paper. We sincerely thank dr. Marta Bolgan for a critical reading and dr.

References (109)

  • G. La Manna et al.

    Behavioural response of brown meagre (Sciaena umbra) to boat noise

    Mar. Pollut. Bull.

    (2016)
  • S. Menegon et al.

    Addressing cumulative effects, maritime conflicts and ecosystem services threats through MSP-oriented geospatial webtools

    Ocean Coast. Manag.

    (2018)
  • S.L. Nedelec et al.

    Repeated exposure to noise increases tolerance in a coral reef fish

    Environ. Pollut.

    (2016)
  • A. Newton et al.

    An overview of ecological status, vulnerability and future perspectives of European large shallow, semi-enclosed coastal systems, lagoons and transitional waters

    Estuar. Coast. Shelf Sci.

    (2014)
  • M. Picciulin et al.

    In-situ behavioral responses to boat noise exposure of Gobius cruentatus (Gmelin, 1789; fam. Gobiidae) and Chromis chromis (Linnaeus, 1758; fam. Pomacentridae) living in a marine protected area

    J. Exp. Mar. Biol. Ecol.

    (2010)
  • M. Picciulin et al.

    Passive acoustic monitoring of Sciaena umbra on rocky habitats in the venetian littoral zone

    Fish. Res.

    (2013)
  • N. Pieretti et al.

    Anthropogenic noise and biological sounds in a heavily industrialized coastal area (Gulf of Naples, Mediterranean Sea)

    Mar. Environ. Res.

    (2020)
  • F. Pranovi et al.

    Recreational fishing on the west coast of the northern Adriatic Sea (Western Mediterranean) and its possible ecological implications

    Reg. Stud. Mar. Sci.

    (2016)
  • N. Rako-Gospić et al.

    Underwater noise: sources and effects on marine life

  • H. Slabbekoorn et al.

    A noisy spring: the impact of globally rising underwater sound levels on fish

    TREE

    (2010)
  • J. Alós et al.

    Experimental acoustic telemetry experiment reveals strong site fidelity during the sexual resting period of wild brown meagre, Sciaena umbra

    J. Appl. Ichthyol.

    (2012)
  • M.C.P. Amorim et al.

    Boat noise impacts lusitanian toadfish breeding males and reproductive outcome

    Sci. Total Environ.

    (2022)
  • R.K. Andrew et al.

    Ocean ambient sound: comparing the 1960s with the 1990s for a receiver off the California coast

    Acoust. Res. Lett. Online

    (2002)
  • T.C. Barnes et al.

    Dispersal of an exploited demersal fish species (Argyrosomus japonicus, Sciaenidae) inferred from satellite telemetry

    Mar. Biol.

    (2019)
  • U. Bergström et al.

    Evaluating eutrophication management scenarios in the Baltic Sea using species distribution modelling

    J. Appl. Ecol.

    (2013)
  • M. Bolgan et al.

    Is the Venice Lagoon Noisy? First Passive Listening Monitoring of the Venice Lagoon: Possible Effects on the Typical Fish Community

    (2016)
  • M. Bolgan et al.

    Fish acoustic community structure in neptune seagrass meadows across the Mediterranean basin

    Aquat. Conserv. Mar. Freshwat. Ecosyst.

    (2022)
  • G. Bombace et al.

    Analysis of the efficacy of artificial reefs located in live different areas of the Adriatic Sea

    Bull. Mar. Sci.

    (1994)
  • C. Bonacito et al.

    Passive hydrophone census of Sciaena umbra (Sciaenidae) in the Gulf of Trieste (Northern Adriatic Sea, Italy)

    Bioacoustics

    (2002)
  • C. Bracciali et al.

    Effects of nautical traffic and noise on foraging patterns of Mediterranean damselfish (Chromis chromis)

    PLoS ONE

    (2012)
  • K. Brander

    Climate and current anthropogenic impacts on fisheries

    Clim. Chang.

    (2013)
  • A. Brazo et al.

    Seasonal influence on the bathymetric distribution of an endangered fish within a marine protected area

    Sci. Rep.

    (2021)
  • K.P. Burnham et al.

    Model Selection and Multimodel Inference: A Practical Information-theoretic Approach

    (2002)
  • G. Buscaino et al.

    Temporal patterns in the soundscape of the shallow waters of a Mediterranean marine protected area

    Sci. Rep.

    (2016)
  • G. Cadiou et al.

    The management of artisanal fishing within the marine protected area of the port-cros National Park (northwest Mediterranean Sea): a success story? ICES

    J. Mar. Sci.

    (2009)
  • F. Cavraro et al.

    Body condition in fish as a tool to detect the effects of anthropogenic pressures in transitional waters

    Aquat. Ecol.

    (2019)
  • G. Cecconi et al.
  • L. Chao

    Sciaena umbra

  • L.N. Chao et al.

    Sciaenidae

  • E. Charbonnel et al.

    Effects of increased habitat complexity on fish assemblages associated with large artificial reef units (French Mediterranean coast)

    ICES J. Mar. Sci.

    (2002)
  • S. Colla et al.

    Using passive acoustics to assess habitat selection by the brown meagre Sciaena umbra in a northern Adriatic Sea mussel farm

    J. Fish Biol.

    (2018)
  • M.A. Connaughton et al.

    Drumming, courtship and spawning behavior in captive weakfish, Cynoscion regalis

    Copeia

    (1996)
  • L. Di Iorio et al.

    Spatio-temporal Surveys of the Brown Meagre Sciaena Umbra Using Passive Acoustics for Management and Conservation

    (2020)
  • C.M. Duarte et al.

    The soundscape of the Anthropocene Ocean

    Science

    (2021)
  • M. Elliott et al.

    Fishes in Estuaries

    (2002)
  • C. Erbe et al.

    Mapping cumulative noise from shipping to inform marine spatial planning

    J. Acoust. Soc. Am.

    (2012)
  • G. Fabi et al.

    Effects on fish community induced by installation of two gas platforms in the Adriatic Sea

    Mar. Ecol. Prog. Ser.

    (2004)
  • C. Ferrarin et al.

    SHYFEM Model Velocity Fields for the Venice Lagoon, Link to NetCDF Files

    (2016)
  • R. Fiorin et al.

    Il popolamento ittico e macroalgale delle scogliere del litorale veneziano: interazione tra le alghe brune del genere cystoseira e alcune specie di pesci

    Biol. Mar. Mediterr.

    (2008)
  • A. Franco et al.

    Environmental influences on fish assemblage in the Venice Lagoon, Italy

    Chem. Ecol.

    (2006)
  • Cited by (0)

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