In situ behavioural 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

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Abstract

The short-term behavioural effects of two types of boat noise were tested on Gobius cruentatus and Chromis chromis, i.e. one permanently and one temporarily benthic vocal fish species living inside the WWF-Natural Miramare Marine Reserve (Northern Adriatic Sea, Italy). The underwater noises produced by a 26-m tourist ferry and a 5-m fiberglass boat were recorded inside the core zone of the reserve. Each type of boat noise was subsequently played back in situ to 10 animals per species (C. chromis males caring their nests or G. cruentatus in their shelters).

The 1/3 octave spectra of recorded sound pressure levels were compared to the underwater ambient noise level and to sound pressure level measured at the hearing threshold of the two species. The boat noise levels have been calculated in terms of particle acceleration for both field measurements and in situ playback projections and subsequently compared to the available measured values of particle acceleration at the hearing threshold.

The animals were free to move in all directions during the whole experimental session. The behaviour of each fish was videotaped by an underwater camera for a total of 10 min (5 min before and 5 min during the noise playback). No short-term behavioural reaction (aversion) was observed in any of the specimen of the two species during the playback of the recorded noises, therefore suggesting no impact. However a time-budget analysis revealed a significant change in the total time spent in caring their nests (C. chromis) or inside their shelters (G. cruentatus). This result highlighted how analyzing fish reaction on a short-term might underestimate the effects of noise disturbance and indicated that the overall fish behaviour should be considered to assess noise impact.

Introduction

Worldwide concern about the impact of noise pollution on aquatic fauna is growing in these years. There is an increasing amount of scientific evidence that anthropogenic noise can harm marine species (Tyack, 2008). While noise pollution has been recognised to be steadily growing in the world's oceans (Andrew et al., 2002), this phenomenon is still largely unmonitored in coastal areas. A major source of low-frequency noise (under 1000 Hz) in marine species living in highly anthropized coastal areas comes from boats and vessels, since their number, distribution and mobility are very high (Greene and Moore, 1995, Richardson and Würsig, 1997).

Boat noise represents a chronic source of harassment (Haviland-Howell et al., 2007) for fish species (Popper, 2003), whose communication for inter- and intra-sexual selection is mainly based on low-frequency sound signals (Ladich and Myrberg, 2006, Myrberg and Lugli, 2006). It has been recently shown that boat noise may induce endocrine stress response (Wysocki et al., 2006), as well as diminish hearing ability and mask intra-specific relevant signals in exposed fish species (Scholik and Yan, 2002, Amoser et al., 2004, Vasconcelos et al., 2007, Codarin et al., 2009). In addition, boat and vessel noises have the capacity to provoke short-term changes in the spatial position and group structure of pelagic fish in the water column, as shown by many studies carried out since the 1960s (for example, Buerkle, 1974, Olsen et al., 1983, Schwarz and Greer, 1984, Engås et al., 1995, Soria et al., 1996, Vabø et al., 2002, Mitson and Knudsen, 2003, Ona et al., 2007, Sarà et al., 2007). The most common boat-induced behavioural changes in fish include the temporary cessation of activities, alarm response, flight reaction or the so-called ‘startle’ response, i.e. a powerful flexion of the body followed by a few seconds of faster swimming (Boussard, 1981). In many species, fish behaviour is affected by noise only when a certain threshold in pressure level is reached. Very often, the previously mentioned short-term changes in swimming speed have been used to fix the threshold of fish behavioural reaction to human noise (Kastelein et al., 2008a), but such noise-response studies on marine fish are rare (Akamatsu et al., 1996) and they show marked differences in the reaction of various species, depending on the threshold levels of the noise frequencies, the threshold levels at which a reaction occurs varying per frequency for each species (Kastelein et al., 2008b). The relationship between the strength of short-term responses and the underlying sensitivity of wildlife is unlikely to be straightforward (Gill et al., 2001) and fish reactions depend not only on the properties of noise but also on the individual context (e.g. location, temperature, physiological state, age, body size, etc.). As result, much more information is still needed to understand the behavioural consequences of anthropogenic noise exposure (Popper et al., 2004).

Interestingly, the application of a time-budget analysis has recently proved to be a useful tool for assessing human disturbance in several cetacean species (e.g., Williams et al., 2006, Hodgson and Marsh, 2007, Dans et al., 2008, Stockin et al., 2008). This technique has never been applied to fish species so far, therefore, the aim of this study was (1) to record, inside a core zone of a coastal reserve, the noise produced by a tourist ferry and a fiberglass boat moving along and inside the Marine Protected Area (MPA); (2) to field-test, through the time-budget method, short-term effects of both boat noise types on a permanently and a temporarily benthic soniferous fish species (Gobius cruentatus and Chromis chromis) living inside the MPA.

Investigating the impact of boat noise on target fish species is particularly relevant for coastal MPAs, which are biologically rich locations in highly populated regions and deserve protection from anthropogenic pollutants. Managers of MPAs have recently begun to study noise (Agardy et al., 2007, Haren, 2007) but far too little is known about animals hearing capacity, behaviour and ecology to set a standard or apply an exposure limit with confidence (Popper and Løkkeborg, 2008). This high level of uncertainty underlines the need for local assessment in noise pollution as well as a precautionary principle as management rule for sensitive areas (Horowitz and Jasny, 2007).

Section snippets

Study area

The field-work has been run at the WWF-Miramare Natural Marine Reserve, an UNESCO-MAB Biosphere Reserve located in the Gulf of Trieste (Northern Adriatic Sea, Italy) at 45°42′08″ N and 13°42′42″ E. The area is divided in a core (30 ha) and in a buffer zone where the maximum depth reaches 18 m. The level of human presence around Miramare MPA is extremely high compared to more remote Mediterranean MPAs. The site is less than 8 km away from the city of Trieste, an important seaport with more than 48 

Boat noise characterization

The equivalent continuous SPL (LLeq, 25 s) of the tourist ferry (TF, recorded at 82 m of distance) and the fiberglass boat (FB, recorded at 1 m of distance) were 140.3 and 158.8 dB re 1 µPa, with a maximum instantaneous SPL of 147.7 and 162.2 dB re 1 µPa, respectively. Assuming a cylindrical spreading (10 log R, meaning a loss of 3 dB per doubling of distance) as the best transmission loss model in shallow water (Richardson et al., 1995), the source level of TF noise can be estimated 160 dB re 1 µPa at 1 

Discussion

Vessel traffic noise dominates the sea ambient noise of coastal areas mainly below 1 kHz (Richardson and Würsig, 1997). Although being extremely variable in relation to speed, load, pitch angle of propeller, vessel design and age (Mitson, 1993, Richardson et al., 1995), boat source level (i.e. the amount of radiated sound measured at 1 m from the source, SL) generally ranges from 145 to 170 dB re 1 µPa at 1 m, with an average of 162 dB re 1 µPa at 1 m for speeds of around 50 km/h (Boussard, 1981, Greene

Acknowledgments

We would like to thank Dr. Maurizio Spoto and the Natural Marine Reserve Miramare staff for the technical assistance and two anonymous referees for valuable comments on the present manuscript. This research was supported by the Italian Ministry for Environment, Territory and Sea. [SS]

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