Boat-induced pressure does not influence breeding site selection of a vulnerable fish species in a highly anthropized coastal area
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.
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These authors contributed equally to this work.