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received: 18 May 2016 accepted: 30 August 2016 Published: 28 September 2016
Temporal patterns in the soundscape of the shallow waters of a Mediterranean marine protected area Giuseppa Buscaino1, Maria Ceraulo1,2, Nadia Pieretti2, Valentina Corrias1, Almo Farina 2, Francesco Filiciotto1, Vincenzo Maccarrone 1, Rosario Grammauta1, Francesco Caruso1, Alonge Giuseppe3 & Salvatore Mazzola1 The study of marine soundscapes is an emerging field of research that contributes important information about biological compositions and environmental conditions. The seasonal and circadian soundscape trends of a marine protected area (MPA) in the Mediterranean Sea have been studied for one year using an autonomous acoustic recorder. Frequencies less than 1 kHz are dominated by noise generated by waves and are louder during the winter; conversely, higher frequencies (4–96 kHz) are dominated by snapping shrimp, which increase their acoustic activity at night during the summer. Fish choruses, below 2 kHz, characterize the soundscape at sunset during the summer. Because there are 13 vessel passages per hour on average, causing acoustic interference with fish choruses 46% of the time, this MPA cannot be considered to be protected from noise. On the basis of the high seasonal variability of the soundscape components, this study proposes a one-year acoustic monitoring protocol using the soundscape methodology approach and discusses the concept of MPA size. Soundscape analysis is an emerging field of ecological research1 that contributes information about biological compositions and environmental conditions. In marine ecosystems, studies have underlined the importance of the acoustic environment to provide information about the quality and types of species habitats2–5. The acoustic environment of a given habitat, or “soundscape”, includes the sounds produced by biotic, abiotic and anthropogenic activity6. These three components, defined as biophony, geophony and anthropophony, interact with each other and determine the peculiar and distinct underwater sound signatures5,7,8, which show a recognizable temporal pattern on daily and seasonal time scales6,9. In marine shallow waters, biophonies are produced by fish, invertebrates and marine mammals. Marine animals emit sounds mainly for communication, and environmental recognition. In some cases, animals generate sounds involuntary during other activities (e.g., during swimming, grazing or shell movement). All these sounds contribute to the biophonic component of a particular soundscape10–12. Vocal fishes produce impulsive or frequency-modulated sounds at low frequencies and low amplitudes, with differences in the duration and number of pulse trains for each species13. Invertebrates, such as shrimp, lobsters and bivalves, emit voluntary or involuntary impulsive and cracking broadband signals10,14,15. In coral reefs, snapping shrimp produce the dominant acoustic energy and exhibit clear daily acoustic trends16. These benthic-dwelling shrimp produce wideband pulses from 3 to 100 kHz, with an irregular pulse repetition rate14, which results from the rapid closing of their enlarged claws and the consequent collapsing cavitation bubble17. Marine mammals in Mediterranean coastal habitats, such as bottlenose dolphins, use two types of sound: broadband impulsive signals (clicks/burst), ranging from a few kHz up to 120 kHz18, and modulated narrowband whistles19,20. Biological sources included in a characteristic soundscape can be either transient21,22, show seasonal patterns11 or be resident21. Moreover, the occurrence of acoustic signals can be related to different ecological 1 National Research Council – Institute for Coastal Marine Environment – Bioacousticslab Capo Granitola, Via del Mare, 6 – 91021 Torretta Granitola, Campobello di Mazara (TP), Italy. 2Department of Pure and Applied Sciences (DiSPeA) – University of Urbino– Campus Scientifico “Enrico Mattei”– 61029 Urbino, Italy. 3ENEA – Observations and Analyses of Earth and Climate – Via Principe di Granatelli, 24 – 90139 Palermo, Italy. Correspondence and requests for materials should be addressed to G.B. (email:
[email protected])
Scientific Reports | 6:34230 | DOI: 10.1038/srep34230
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www.nature.com/scientificreports/ processes, such as reproduction, agonistic and territorial displays, detection of predators, searching and foraging for prey, orientation and navigation, and group cohesion6,15,23–25. The abiotic sounds in coastal areas are determined by winds and waves, including breaking surface waves11, rainfall26, and waves beating against cliffs. The wind contribution dominates from a few Hz to 30 kHz, and surface waves cause mostly infrasonic noise at frequencies from 10 to 100 Hz11. The two sources are related, although surf noise, which is defined as wave noise localized near the land-sea surface, is prominent, even in calm wind conditions. Rainfall also produces energy peaks from 15–20 kHz27, while thunder and lighting generate sounds at lower frequencies, which contribute to background noise even if the storm is distant28. Anthropogenic noise in coastal areas is mainly due to vessel traffic29, particularly at low frequencies (10 years), large (>100 km2), and isolated from deep water or sand41. Increasing the size of no-take zone increases the density of commercial fish within the reserve compared to out side42. The MPA “Pelagie Islands” is located in the Strait of Sicily (see Fig. 1), which divides the Eastern and Western Mediterranean basins and divides Africa from Europe. The Sicilian Channel is considered an area of high biogeographical43 and hydrodynamic importance44, and it can be regarded as a privileged observatory for biodiversity monitoring45. The Pelagie Islands are an asset for the biodiversity of the Mediterranean. In their coastal waters, vulnerable (fin whale, bottlenose dolphin), endangered (common dolphin), and near-threatened species (brown meagre, Sciaena umbra) (IUCN Global Species Programme Red List Unit) live and/or migrate. Some authors45 have characterized the littoral fish assemblage of Lampedusa (the biggest island of the Pelagie Archipelago) to create a reference against which changes in the Mediterranean rocky-reef fish assemblage can be assessed in the future. In Lampedusa (Fig. 1), 23 families and 61 taxa of fishes have been recorded45, with a predominance of Labridae, including sonoriferous fishes, such as Chromis chromis, Sciaena umbra, and Gobidae. Galatheidae, Hyppolytidae and the three sonoriferous species of snapping shrimp belonging to the Alpheidae family (Alpheus dentipes, Alpheus macrocheles, and Synalpheus gambarelloides) have also been included in a checklist study46 on the decapod crustaceans living in Lampedusa from 0 to 30 m depth in rock and in the Posidonia oceanica substratum. Characterization and evaluation of the contributions of natural and anthropogenic sources and identification of the ecological dynamics are crucial elements for assessing the impact of man-made disturbances on marine habitats11,30. The European Union Marine Strategy Framework Directive (MSFD)(2008/56/EC) promotes the achievement of a good quality environmental status for European waters by 2020. In particular, Descriptor 11.2 about “continuous low frequency sound” aims to monitor trends in the ambient noise level within the 1/3 octave bands47 of 63 and 125 Hz (centre frequencies) (re 1 μΡa rms). To obtain a baseline to develop a noise-monitoring plan in marine shallow waters (i.e., how long should the monitoring last? How many recording stations are needed to appropriately detect the spatial variability in the soundscape components? How do biological sound sources contribute to the noise level? How do the different soundscape components change in different seasons?), a one-year octave band analysis could provide a useful indication of the seasonal and circadian variability of the levels of noise and contribute to the detection of possible sources of noise, distinguishing them as anthropogenic or non-anthropogenic. In recent years, automated tools and new ecoacoustic metrics have enabled the quantification of the amount of sound and the estimation of the level of biodiversity in terrestrial environments using large datasets48. For example, ecoacoustic metrics have been successfully used to study the alteration of singing dynamics caused by traffic noise49. These automatic procedures have the potential to provide useful insight when working with marine acoustic recordings, but until now, very few studies have applied these methodologies to the underwater world5. This study explores the shallow water soundscape of an MPA in the central Mediterranean Sea (Lampedusa Island) over an entire year. The main aims were to a) investigate the seasonal and circadian patterns of octave band sound pressure levels (BPLs), b) identify the principal biological, physical and anthropogenic sound sources c) test the acoustic complexity index48 (ACI) as an automated metric to describe the biotic contribution to the soundscape, and d) quantify the percentage of time in which fish choruses are masked by vessel passage noise.
Scientific Reports | 6:34230 | DOI: 10.1038/srep34230
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Figure 1. Top: The study area (red arrow) at two scales: Topleft-Lampedusa Island in the Central Mediterranean Sea; Topright-Lampedusa Marine Protected Area (red arrow). Below: Capo Grecale MPA delimited by yellow buoys with the spacing shown. The recorder position (red point) was near the midpoint of the MPA. (Map source: Schlitzer, R., Ocean Data View, odv.awi.de, 2015).
Results
Table 1 summarizes the results of the BPL analysis for different seasons, distinguishing daytime (12:00 pm ± 2 hours), night-time (12:00 am ± 2 hours) or 24 hours. Figure 2 shows the monthly trends of the BPLs for the lower and higher frequencies. The BPLs at lower frequencies (Fig. 2a, from 63 Hz to 1000 Hz) increased from November to March. The higher frequencies (Fig. 2b, from 2 kHz to 64 kHz) followed the opposite pattern, with lower values during the winter. This difference in trends is appreciable in Fig. 3, in which the one-year mean power spectrum (black line) and the summer and winter mean power spectra (blue and grey lines, respectively) are shown. For the lower frequency (62 Hz), the difference between the winter and summer BPLs was 5.9 dB (respectively, 103.7 and 97.8 dB re 1 μPa, see Table 1), and for the higher frequency (i.e., 8 kHz) the mean difference between winter and summer was 8.6 dB (respectively, 102.3 and 110.9 dB re 1 μPa, see Table 1). This seasonal variability was mainly attributable to the sea state for the lower frequencies and to the activity of snapping shrimp for the higher frequencies (see Table 2, Figs 4 and 5). The total band sound pressure level is much more stable over seasons and with the circadian cycle (see Table 1). Figure 3 also shows a “stability” band centred at 2 kHz, which has a mostly stable and lower BPL throughout the year. This can be explained by the correlation values between BPLs at 2 kHz and the main components of the soundscape in Table 2. Excluding the anthropophony, a very low level of correlation of biophony and geophony vs. BPL at 2 kHz was found (Table 2). In Fig. 4, the median power spectra for the night-time hours and daytime hours are shown for all seasons. Circadian patterns are more evident during the summer, both for the higher and the lower frequencies. During the other seasons, it is possible to distinguish some small differences (approximately 2 dB) between night and day only for the higher frequencies (from 4 kHz). In Fig. 5, the mean circadian trends for the BPL and ACI values
Scientific Reports | 6:34230 | DOI: 10.1038/srep34230
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One Year 24 hours m.
10% 90%
Summer
day m.
10% 90%
night m.
10% 90%
24 hours m.
Autum
day
10% 90%
m.
night
10% 90%
m.
24 hours
10% 90%
m.
10% 90%
Winter
day m.
night
10% 90%
m.
24 hours
10% 90%
m.
Spring
day
10% 90%
m.
night
10% 90%
m.
24 hours
10% 90%
m.
10% 90%
day m.
10% 90%
night m.
10% 90%
62.5 Hz 101.6
93.4 109.9 101.8 94.0 110.1 101.0 92.5 109.7 97.8
91.4
106.7 99.0
93.0
107.4
95.8
90.3
105.9 100.0
90.9 110.0 99.6
90.8
110.0
99.8
90.0
109.5 103.7 96.6 112.3 103.5 96.3 113.4 95.8
90.3
105.9 103.0
96.6 109.7 103.1 96.7 109.4 102.4 96.2 109.9
125 Hz
100.9
91.9 107.8 101.0 92.5 107.7 100.7 90.6 107.7 96.8
88.9
104.8 97.7
90.5
105.0
94.8
87.5
103.5
98.9
88.8 107.7 97.9
88.0
106.7
99.4
89.3
107.8 102.9 97.0 109.5 102.7 96.9 111.4 94.8
87.5
103.5 102.0
95.9 107.9 102.2 95.9 107.6 102.1 95.8 108.6
250 Hz
101.7
92.9 107.1 101.6 93.1 107.3 101.6 91.5 106.9 98.3
90.1
105.0 98.6
91.4
105.0
96.1
89.0
104.0 100.2
91.2 106.8 99.5
90.8
105.9 100.7
90.2
107.0 103.3 98.0 108.6 103.3 97.2 112.5 96.1
89.0
104.0 102.3
95.9 107.3 102.3 96.2 106.9 102.5 95.9 107.7
500 Hz
100.9
93.3 105.8 100.8 93.8 105.7 100.9 92.3 105.5 97.8
89.9
104.4 97.8
91.1
104.4
96.7
88.8
103.8
99.9
93.8 106.2 99.2
93.7
105.6 100.2
92.8
106.4 102.6 98.3 107.1 102.5 97.5 110.5 96.7
88.8
103.8 101.0
95.2 105.1 101.1 95.1 104.9 101.2 95.4 105.2
1 kHz
98.6
92.7 104.4 98.4
92.6 104.2 98.6
92.6 104.2 96.9
91.0
104.0 96.2
91.0
103.2
96.9
91.4
103.5
97.5
93.2 104.4 96.9
93.0
103.9
97.7
92.4
104.6 100.3 95.3 105.9 99.9
94.7 109.1 96.9
91.4
103.5
98.3
92.5 103.3 98.8
92.4 102.6 98.3
92.9 103.6
2 kHz
99.3
95.4 103.0 98.8
95.2 103.2 99.7
95.5 102.8 100.4 97.9
103.0 99.5
97.1
103.5 101.1 99.0
102.9
97 8
95.0 101.9 96.8
94.2
101.6
97.9
95.2
101.7
94.6 105.7 101.1
99.0
102.9
99.0
96.0 102.5 98.7
95.9 101.8 99.3
96.1 102.8
4 kHz
104.1 100.3 109.7 103.3 99.7 108.0 105.0 100.7 110.3 108.4 105.4 111.5 107.1 104.4 110.8 109.9 107.5 111.8 104.1 101.2 107.4 103.2
99.8
104.8 105.2 101.9 107.3 101.3 99.3 104.1 100.8 98.5 104.8 109.9 107.5 111.8 104.2 101.4 107.4 103.0 100.5 106.4 105.0 102.4 107.6
98.8
94.4 104.2 98.6
8 kHz
107.1 102.8 112.0 105.7 101.8 109.9 108.5 103.6 112.8 110.9 107.8 113.4 109.2 106.9 111.5 112.4 110.8 114.0 107.7 104.5 111.2 106.5 103.0 108.1 109.4 106.0 111.2 103.7 101.6 105.7 102.3 100.8 104.5 112.4 110.8 114.0 107.2 104.2 110.4 105.6 103.0 108.7 108.4 105.7 110.6
16 kHz
107.2 102.8 112.3 105.4 101.6 109.6 108.5 104.0 113.0 110.5 108.0 113.6 109.1 107.0 110.4 112.8 111.2 113.9 108.3 104.7 112.2 106.8 103.2 108.8 110.2 106.7 112.4 103.9 101.5 105.9 102.1 100.4 103.9 112.8 111.2 113.9 107.2 103.9 110.3 105.4 102.7 108.2 108.4 105.9 110.5
32 kHz
105.2 100.8 110.3 103.2 99.3 107.4 106.7 102.2 111.1 108.4 105.8 111.6 106.9 104.9 108.6 110.7 108.9 112.2 106.6 102.6 110.5 105.0 101.2 107.1 108.5 105.3 110.8 101.9 99.3 104.1 99.9
98.3 101.7 110.7 108.9 112.2 105.1 101.9 108.1 103.1 100.5 106.0 106.4 104.1 108.4
64 kHz
100.6
94.7
Total band
96.6 105.5 98.7
95.4 102.8 102.1 98.0 106.4 103.7 100.7 107.0 101.7 100.1 104.2 105.7 103.8 107.6 102.0
98.2 105.7 100.6
96.9
102.3 103.8 101.0 106.1
97.7
95.4
99.9
95.9
97.4 105.7 103.8 107.6 100.5
97.6 103.6 98.6
96.4 101.0 101.8 99.6 103.6
116.3 112.7 121.2 115.6 112.1 121.2 117.3 112.9 121.4 117.9 115.6 120.1 116.1 115.3 119.5 118.7 117.8 120.2 116.5 114.2 120.6 115.0 113.7 120.2 117.0 115.0 120.5 114.5 111.5 122.4 114.0 110.9 123.2 118.7 117.8 120.2 115.8 113.2 122.2 115.0 112.5 121.9 116.3 113.7 122.7
Table 1. rms octave band sound pressure level (Median, 10thpercentile, 90thpercentile) calculated for one year, for all seasons, for 24 hours, for the day (10:00 am−3:00 pm) and at night (10:00 pm−3:00 am).
Figure 2. Seasonal trends (one year of data from July 2013 until June 2014) in the rms octave band sound pressure levels (BPL) for different frequencies. (a) Lower frequency BPL (from 62.5 to 1000 Hz). (b) Higherfrequency BPL from 2 kHz to 64 kHz. (Median; Whisker: 40th–60th).
for each month of the year are shown for three selected frequency bands (centred at 250 Hz, 1 kHz and 4 kHz). Figure 5a,b show the mean numbers of counted vocalizations per minute produced by fish (the grey area). The fish counting peaks at sunset for 250 Hz and 1 kHz are in line with the ACI peaks (blue line) and with the correlations in the octave bands occupied by fish sounds (as shown in Table 2). The BPLs (black line) showed the Scientific Reports | 6:34230 | DOI: 10.1038/srep34230
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Figure 3. Seasonal trends of rms BPLs for all data (one year), summer data (July, August and September) and winter data (December, January and February)(Median; Whisker: 45th–55th percentile). The differences between the summer and winter for each BPL are significant (Mann-Whitney U test, p
