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Acoustic characteristics of two feeding modes used by brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and turbot (Scophthalmus maximus)
Aquaculture 240 (2004) 607 – 616 www.elsevier.com/locate/aqua-online
Short communication
Acoustic characteristics of two feeding modes used by brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and turbot (Scophthalmus maximus) J.P. Lagarde`re a,*, R. Mallekh b, A. Mariani c b
a CNRS-IREMER, CREMA L’Houmeau, B.P. 5, 17137 L’Houmeau, France Faculte´ des Sciences de Sfax, De´partement de Biologie, B.P. 802, 3018 Sfax, Tunisia c CNRS, Centre d’Etudes Biologiques de Chize´, 79360 Villiers-en-Bois, France
Received 8 September 2003; received in revised form 21 January 2004; accepted 21 January 2004
Abstract Under conditions of intensive culture, the acoustic signals produced by fish during feeding depend on their feeding mode. Exclusive suction, as used by turbot, is characterised by a maximum acoustic energy in the frequency range 7 – 9 kHz and a sound duration of about one minute depending of time duration of pellet distribution. Suction feeding in conjunction with forward swimming, as employed by brown trout and rainbow trout, had a maximum acoustic energy in the frequency range 4 – 6 kHz and feeding sounds were measurable only for short periods (less than 1 s) in between two pellet distributions by hand. The brevity of these feeding sounds (ca. 1000 ms) requires adapting the turbot acoustic-detection systems to actively feeding fish for developing automated feed distribution systems feasible in trout aquaculture. D 2004 Elsevier B.V. All rights reserved. Keywords: Acoustic characteristics; Feeding mode; Trout; Turbot
1. Introduction Teleosts feed mainly by suction feeding (Muller and Osse, 1984) and ingestion can be achieved by suction exclusively or by suction coupled with swimming. Suction is generated
* Corresponding author. Tel.: +33-546500608; fax: +33-546500600. E-mail address: [email protected] (J.P. Lagarde`re). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.01.033
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J.P. Lagarde`re et al. / Aquaculture 240 (2004) 607–616
by rapid expansion of the buccal and opercular cavities (Osse and Muller, 1980; Van Leeuwen, 1984). Exclusive suction is observed in turbot (Lagarde`re and Mallekh, 2000), carp and other cyprinids (Takemura et al., 1988). The exclusive suction mode of ingestion requires that the fish be near to its prey or feed pellets, but does not require that the fish be in motion (Sibbing et al., 1986 ; Callan and Sanderson, 2003). In turbot culture systems, the entire feeding process from pellet distribution to end of ingestion can take more than 1 min (Mallekh et al., 2003). Suction combined with forward swimming characterises active predators, such as salmonids. Under culture conditions, this feeding mode is generally accompanied by splashing noises and strong tail flips (Phillips, 1989) and ingestion occurs rapidly as the pellets hit the water surface. The objective of our study was to analyse the acoustic characteristics of feeding in fast swimming predators, like brown trout and rainbow trout, and to compare the results with a slow swimming or motionless predator like turbot (Lagarde`re and Mallekh, 2000). Ultimately our goal is to determine the sound frequency range and the time period that is potentially useful for controlling feed distribution in trout culture system, as has been done for turbot (Mallekh et al., 2003).
2. Materials and methods 2.1. Fish Groups of rainbow trout (Oncorhynchus mykiss (Walbaum, 1792)) with a body weight of about 500 –600 g (ca 1300 kg biomass) and brown trout (Salmo trutta Linnaeus, 1758) with a body weight of approximately 600 – 700 g (ca. 800 kg biomass) were used in this study. The fish were held in 6 m diameter circular-concrete tanks of 0.8– 1 m depth, and were hand-fed with Biomar feed pellets (diameter: 6 mm; 5200 pellets/kg). Groups of turbot (Scophthalmus maximus (Linnaeus, 1758)) having a body weight of about 450 – 550 g (ca. 1500 kg biomass) were also recorded. These fish which were reared in concrete tanks (surface area=32 m2 and depth=0.9 – 1 m), were hand-fed with G 7 Gouessant feed pellets (3830 pellets/kg). All fish used in this study were fed 2 meals per day, at approximately 0900 and 1430 h. Feed was distributed by hand, and each handful contained between 200 and 300 pellets. The water temperature in turbot tanks was 15 jC and for trout 14 jC. More details on the feeding and aquaculture conditions can be found in Mallekh et al. (1998). 2.2. Sound recordings and analyses The feeding sounds of trout were recorded at the Salmoniculture Experimentale Marine IFREMER-INRA (SEMII, Sizun, France) during May 2002 and those of turbot at the France Turbot fish farm (Noirmoutier island, France) during the same period.
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Fig. 1. Spectral analysis of food pellets hitting the water in a SEMII tank without fish (—). The dotted line spectrum (: : :) represents the level of background noise in the same tank.
Fig. 2. Feeding sound spectra of medium-sized turbot individuals (400 – 550 g) compared to the background noise spectra in the farming tank before feeding (: : :, lower spectrum), start of feeding (—, upper spectrum) and end of feeding (: : :, medium spectrum).
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Sounds were detected with a hydrophone (Bru¨el and Kjaer, type 8101) having a sensitivity of 184 dB referred to 1 V/APa and with a flat frequency response of up to 120 kHz. The hydrophone was installed in each rearing tank successively, and maintained at about 0.2 m above the tank bottom. It was protected from accidental collision with fish by a cylindrical net. Sound emissions from the hydrophone were calibrated using a Bru¨el and Kjaer calibrator (type 4223). The sound pressure level (SPL) produced in the 8101 coupler volume was 157 dB re 1 APa at a frequency of 250 Hz. The sounds were amplified with a Bru¨el and Kjaer amplifier (type 2610) and recorded with a Sony TCD-D8 digital audio tape-recorder (recording band with : 20– 22 000 HzF1.0 dB). A complete feeding-sequence recording comprised successive recordings of background noise before feeding and background noise plus feeding sounds of each group of fish. Sounds were analysed using a Tektronix 2622 analyser and IP software. Narrowband frequency spectra were obtained with a 1024-point FFT analysis and the average was calculated from 50 samples in each recording. Sonographic analysis of the signals, (previously digitised by a 16-bit acquisition card equipped with an antialiasing filter (low pass filter, fc=11.02 kHz; 120 dB/octave) at a sampling rate of 16 kHz), was conducted with the SYNTANA analytic package (Aubin, 1994; Lengagne et al., 2000).
Fig. 3. Sonogram of pellet noise impact during one hand pellet distribution (ca. 200 – 300 pellets).
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Fig. 4. Feeding sound spectrum of brown trout (—) compared to food-pellet sound spectrum recorded from the tank without fish (: : : ).
Fig. 5. Feeding sound spectrum of rainbow trout (—) compared to food-pellet sound spectrum recorded from the tank without fish (: : : ).
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3. Results 3.1. Description of the underwater ambient noise of culture systems Recorded during non-feeding periods, the background noise characteristics of the SEMII trout culture system were in two low frequency regions: one below 100 Hz, which peaked at 110 dB re 1 APa rms and the second around 400 Hz, which peaked at 92.8 dB re 1 APa rms (Fig. 1). Above 400 Hz, the sound level gradually decreased as the frequency increased and stabilized above 6 kHz at 50 –55 dB re 1 APa rms (Fig. 1, lower dashed spectrum). In the turbot culture system, underwater ambient noise was higher than in the trout culture system: 101 – 105 dB re 1 APa rms below 100 Hz and 96 dB re 1 APa rms around 375 Hz (Fig. 2, lower most dashed spectrum). Above 400 Hz, the ambient sound level decreased and stabilized at 65 dB re 1 APa rms between 7 and 10 kHz. 3.2. Description of the pellet sounds Noise from the impact of feed pellets on the water surface could interfere with feeding sounds (Fig. 1, upper spectrum). The highest energy distribution (in SPL, 83 93 dB re 1 APa rms) was measured in the frequency band between 1 and 2 kHz. Between 2 and 10
Fig. 6. Sonogram of feeding sound produced by brown trout. Note absence of feeding sounds before impact of pellets hitting water surface.
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kHz, the sound pressure level exceeded the underwater ambient noise level by at least 10 dB. The duration of this effect was between 200 and 600 ms (Fig. 3); the feed was distributed manually, and thus there may have been some variability in the number of feed pellets distributed each time and in their dispersion within the tank. 3.3. Description of the feeding sounds For both trout species, feeding activity starts as feed pellets hit the water surface but, within the 0 – 2 kHz frequency band, feeding sounds are masked by pellet impacts on the water surface (Figs. 4 and 5). For brown trout, feeding sounds are clearly distinguishable from ambient noise between 2.5 and 4 kHz (Fig. 4) and between 4 and 10 kHz, the acoustic energy decreases. The signal/noise ratio reached a maximum (about 15 dB) between 4 and 7 kHz. Sonograms (Fig. 6) confirmed the rapidity of the brown trout’s reaction to distributed feed: the average duration of feeding (including feed throw) was about 1400 ms, whereas the throwing periodicity was about 1800 ms. For rainbow trout (Fig. 5), the frequency band in which feeding activity can be clearly distinguished was from 2 to 5 kHz and the highest signal/noise ratio recorded was between 4 and 6 kHz (15 – 20 dB). Turbot feeding lasted longer than the trout. Pellet suctions take place after a few handfuls of pellets hit the water surface, thus representing the required time to stimulate
Fig. 7. Sonogram of feeding sound produced by the turbot. Suction feeding noises are observed before and after pellet impacts on water surface.
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Fig. 8. Comparison of feeding sound spectra of brown trout (: : : , lower spectrum), rainbow trout (: : :, medium spectrum), and turbot (—, upper spectrum) in farming environment.
fish feeding. Suctions intensified and then decreased over approximately one minute. After the stimulation period (ca. 4 – 5 s), the feeding process was continuous between two consecutive pellet distributions (Fig. 7). The sonogram and the narrow-band frequency spectra (Fig. 2) showed that turbot feeding noise is detected over a wide frequency band of up to 10 kHz or more. Between 3 and 9 kHz, the sound level reached 80– 90 dB re 1 APa rms and the corresponding signal/noise ratio was between 15 and 20 dB. Comparisons between the feeding noise spectra of these three fish species indicate that their frequency spectra are similar within the 2 –5 kHz frequency band (Fig. 8), but differ within the 7 – 9 kHz frequency band.
4. Discussion In aquaculture systems, low frequency noise (
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higher frequency band, the two feeding strategies analysed (suction (turbot) and suction+ forward swimming (trout)) were easily identifiable. Under culture conditions, the feeding behaviours of the two trout species are different: rainbow trout pick up pellets at the water surface, whereas brown trout ingest pellets under the water surface. However, in spite of this difference, their feeding sounds are similar. For both trout species, the maximum feeding signal/noise ratio was observed between 4 and 6 kHz. This same frequency band is also observed in feeding and swimming noise studies of other species such as the: Atlantic horse mackerel (1.6 –4 kHz; Shishkova, 1958), Japanese horse mackerel (0.6 –8 kHz; Kaparang et al., 1999), yellowtail (4– 6 kHz; Takemura et al., 1988), and the yellowtail and amberjack (4– 8 kHz; Kaparang et al., 1998). For feeding turbot, the maximum signal/noise ratio observed was between 6 and 9 kHz at 15– 20 dB and was consistent with our previous results (Lagarde`re and Mallekh, 2000). The comparison between turbot and trout showed that frequency spectra were similar within the frequency band of 2 – 5 kHz. The 7– 9 kHz frequency band seems to be characteristic of feeding turbot and, furthermore of the exclusive suction feeding mode. This hypothesis is supported by the observations of Takemura et al. (1988) made during carp feeding behaviour study. In this species, which also uses an exclusive suction feeding mode, the high frequency band (4– 9 kHz) characterised feeding activity and showed a maximum acoustic energy between 7 and 9 kHz. Mallekh et al. (2003) indicated that the acoustic characteristics of feeding sounds may be potentially useful for controlling feed distribution in aquaculture. In turbot culture systems, this interest is not only due to the fact that acoustic energy varies over periods of more or less than 1 min depending on the variation in feeding intensity, but also to the nonalteration of the frequency band that characterises the turbot feeding sounds (7 –9 kHz) by environmental noises. The use of feeding sounds of active predators, such as trout, will be more difficult. First, the rapid pellet capture by these species superimposes feeding sounds and pellet impacts, in addition to noise related to variations in swimming speed and splashing. Nonetheless, a suitable signal could be used within the short time between consecutive feed distributions (ca. 1000 ms). Secondly, the frequency range limitation of the feeding sounds (20 –6000 Hz) presents some practical issues. The 20– 400 Hz frequency band is inappropriate for aquaculture applications since it is masked by the ambient noise of land based aquaculture systems (water flows, pumps, aerator, etc.) or to noise related to variation of atmospheric parameters in rearing conditions at sea (Wenz, 1962; Urick, 1983; Zakarauskas, 1986 ; Lagarde`re et al., 1994). The 4– 6 kHz frequency band offers the best opportunity for detection of feeding activity because it has a weak interference with the noise of land based aquaculture systems, however these frequencies could be masked by meteorological noise (rainfall, wind, etc.) in the outdoor ponds or enclosures.
Acknowledgements This study was financially supported by the ‘‘Cellule de Valorisation de la Recherche du CNRS’’ and the ‘‘Conseil Re´gional de Poitou-Charentes’’. We wish to thank J. Guarini for improving the language.
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References Aubin, T., 1994. Syntana: a software for the synthesis analysis of animal sounds. Bioacoustics 6, 80 – 81. Bart, A.N., Clark, J., Young, J., Zohar, Y., 2001. Underwater ambient noise measurements in aquaculture systems: a survey. Aquac. Eng. 25, 99 – 110. Callan, W.T., Sanderson, S.L., 2003. Feeding mechanisms in carp: crossflow filtration, palatal protrusions and flow reversals. J. Exp. Biol. 206, 883 – 892. Fujieda, S., Matsuno, Y., Yamanaka, Y., Chung, Y., Kishimoto, C., 1993. Feature of the swimming sound for fishes in the netting cages at the culture ground. Mem. Fac. Fish., Kagoshima Univ. 42, 1 – 9. Kaparang, F.E., Matsuno, Y., Yamanaka, Y., Fujieda, S., 1998. Studies on underwater sounds produced by yellowtail Seriola quinqueradiata and amberjack Seriola dumerili in net pens at culture grounds in middle Kagoshima Bay. Fisheries Sci. 64, 353 – 358. Kaparang, F.E., Matsuno, Y., Yamanaka, Y., Fujieda, S., 1999. Studies on underwater sounds produced by Japanese horse mackerel Trachurus japonicus in net pens at culture grounds in innermost Kagoshima Bay. Fish. Sci. 65, 398 – 404. Lagarde`re, J.P., Mallekh, R., 2000. Feeding sounds of turbot (Scophthalmus maximus) and their potential use in the control of food supply in aquaculture: I. Spectrum analysis of the feeding sounds. Aquaculture 189, 251 – 258. Lagarde`re, J.P., Be´gout, M.L., Lafaye, J.Y., Villotte, J.P., 1994. Influence of wind-produced noise on orientation in the sole (Solea solea). Can. J. Fish. Aquat. Sci. 51, 1258 – 1264. Lengagne, T., Aubin, T., Jouventin, P., Lauga, J., 2000. Perceptual salience of individually distinctive features in the calls of adult king penguins. J. Acoust. Soc. Am. 107, 508 – 516. Mallekh, R., Lagarde`re, J.P., Be´gout Anras, M.L., Lafaye, J.Y., 1998. Variability in appetite of turbot, Scophthalmus maximus under intensive rearing conditions: the role of environmental factors. Aquaculture 165, 123 – 138. Mallekh, R., Lagarde`re, J.P., Eneau, J.P., Cloutour, C., 2003. An acoustic detector of turbot feeding activity. Aquaculture 221, 481 – 489. Muller, M., Osse, J.W.M., 1984. Hydrodynamics of suction feeding in fish. Trans. Zool. Soc. Lond. 37, 51 – 135. Osse, J.W.M., Muller, M., 1980. A model of suction feeding in teleostean fishes with some implications for ventilation. In: Ali, M.A. (Ed.), Environmental Physiology of Fishes Plenum, New York, pp. 335 – 352. Phillips, M.J., 1989. The feeding sounds of rainbow trout, Salmo gairdneri Richardson. J. Fish Biol. 35, 589 – 592. Shishkova, E.V., 1958. Notes and investigations on sound produced by fishes. Tr. Vses. Inst. Ribn. Hozaist. Okeanograf. 36, 280 – 294 (in Russian). Sibbing, F.A., Osse, J.W.M., Terlouw, A., 1986. Food handling in the carp (Cyprinus carpio): its movement patterns, mechanisms and limitations. J. Zool. Lond. A 210, 161 – 203. Takemura, A., Nishida, N., Kobayashi, Y., 1988. The attraction of natural feeding sound in fish. Bull. Fac. Fish., Nagasaki Univ. 63, 1 – 4. Urick, R.J., 1983. Principles of Underwater Sound McGraw-Hill, New York. 423 pp. van Leeuwen, J.L., 1984. A quantitative study of flow in prey capture by Rainbow trout, Salmo gairdneri with general consideration of the actinopterygian feeding mechanism. Trans. Zool. Soc. Lond. 37, 171 – 227. Wenz, G.M., 1962. Acoustic ambient noise in the ocean: spectra and sources. J. Acoust. Soc. Am. 34, 1936 – 1956. Zakarauskas, P., 1986. Ambient noise in shallow water: a literature review. Acoust. Can. 14, 3 – 17.
Short communication
Acoustic characteristics of two feeding modes used by brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and turbot (Scophthalmus maximus) J.P. Lagarde`re a,*, R. Mallekh b, A. Mariani c b
a CNRS-IREMER, CREMA L’Houmeau, B.P. 5, 17137 L’Houmeau, France Faculte´ des Sciences de Sfax, De´partement de Biologie, B.P. 802, 3018 Sfax, Tunisia c CNRS, Centre d’Etudes Biologiques de Chize´, 79360 Villiers-en-Bois, France
Received 8 September 2003; received in revised form 21 January 2004; accepted 21 January 2004
Abstract Under conditions of intensive culture, the acoustic signals produced by fish during feeding depend on their feeding mode. Exclusive suction, as used by turbot, is characterised by a maximum acoustic energy in the frequency range 7 – 9 kHz and a sound duration of about one minute depending of time duration of pellet distribution. Suction feeding in conjunction with forward swimming, as employed by brown trout and rainbow trout, had a maximum acoustic energy in the frequency range 4 – 6 kHz and feeding sounds were measurable only for short periods (less than 1 s) in between two pellet distributions by hand. The brevity of these feeding sounds (ca. 1000 ms) requires adapting the turbot acoustic-detection systems to actively feeding fish for developing automated feed distribution systems feasible in trout aquaculture. D 2004 Elsevier B.V. All rights reserved. Keywords: Acoustic characteristics; Feeding mode; Trout; Turbot
1. Introduction Teleosts feed mainly by suction feeding (Muller and Osse, 1984) and ingestion can be achieved by suction exclusively or by suction coupled with swimming. Suction is generated
* Corresponding author. Tel.: +33-546500608; fax: +33-546500600. E-mail address: [email protected] (J.P. Lagarde`re). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.01.033
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J.P. Lagarde`re et al. / Aquaculture 240 (2004) 607–616
by rapid expansion of the buccal and opercular cavities (Osse and Muller, 1980; Van Leeuwen, 1984). Exclusive suction is observed in turbot (Lagarde`re and Mallekh, 2000), carp and other cyprinids (Takemura et al., 1988). The exclusive suction mode of ingestion requires that the fish be near to its prey or feed pellets, but does not require that the fish be in motion (Sibbing et al., 1986 ; Callan and Sanderson, 2003). In turbot culture systems, the entire feeding process from pellet distribution to end of ingestion can take more than 1 min (Mallekh et al., 2003). Suction combined with forward swimming characterises active predators, such as salmonids. Under culture conditions, this feeding mode is generally accompanied by splashing noises and strong tail flips (Phillips, 1989) and ingestion occurs rapidly as the pellets hit the water surface. The objective of our study was to analyse the acoustic characteristics of feeding in fast swimming predators, like brown trout and rainbow trout, and to compare the results with a slow swimming or motionless predator like turbot (Lagarde`re and Mallekh, 2000). Ultimately our goal is to determine the sound frequency range and the time period that is potentially useful for controlling feed distribution in trout culture system, as has been done for turbot (Mallekh et al., 2003).
2. Materials and methods 2.1. Fish Groups of rainbow trout (Oncorhynchus mykiss (Walbaum, 1792)) with a body weight of about 500 –600 g (ca 1300 kg biomass) and brown trout (Salmo trutta Linnaeus, 1758) with a body weight of approximately 600 – 700 g (ca. 800 kg biomass) were used in this study. The fish were held in 6 m diameter circular-concrete tanks of 0.8– 1 m depth, and were hand-fed with Biomar feed pellets (diameter: 6 mm; 5200 pellets/kg). Groups of turbot (Scophthalmus maximus (Linnaeus, 1758)) having a body weight of about 450 – 550 g (ca. 1500 kg biomass) were also recorded. These fish which were reared in concrete tanks (surface area=32 m2 and depth=0.9 – 1 m), were hand-fed with G 7 Gouessant feed pellets (3830 pellets/kg). All fish used in this study were fed 2 meals per day, at approximately 0900 and 1430 h. Feed was distributed by hand, and each handful contained between 200 and 300 pellets. The water temperature in turbot tanks was 15 jC and for trout 14 jC. More details on the feeding and aquaculture conditions can be found in Mallekh et al. (1998). 2.2. Sound recordings and analyses The feeding sounds of trout were recorded at the Salmoniculture Experimentale Marine IFREMER-INRA (SEMII, Sizun, France) during May 2002 and those of turbot at the France Turbot fish farm (Noirmoutier island, France) during the same period.
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Fig. 1. Spectral analysis of food pellets hitting the water in a SEMII tank without fish (—). The dotted line spectrum (: : :) represents the level of background noise in the same tank.
Fig. 2. Feeding sound spectra of medium-sized turbot individuals (400 – 550 g) compared to the background noise spectra in the farming tank before feeding (: : :, lower spectrum), start of feeding (—, upper spectrum) and end of feeding (: : :, medium spectrum).
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Sounds were detected with a hydrophone (Bru¨el and Kjaer, type 8101) having a sensitivity of 184 dB referred to 1 V/APa and with a flat frequency response of up to 120 kHz. The hydrophone was installed in each rearing tank successively, and maintained at about 0.2 m above the tank bottom. It was protected from accidental collision with fish by a cylindrical net. Sound emissions from the hydrophone were calibrated using a Bru¨el and Kjaer calibrator (type 4223). The sound pressure level (SPL) produced in the 8101 coupler volume was 157 dB re 1 APa at a frequency of 250 Hz. The sounds were amplified with a Bru¨el and Kjaer amplifier (type 2610) and recorded with a Sony TCD-D8 digital audio tape-recorder (recording band with : 20– 22 000 HzF1.0 dB). A complete feeding-sequence recording comprised successive recordings of background noise before feeding and background noise plus feeding sounds of each group of fish. Sounds were analysed using a Tektronix 2622 analyser and IP software. Narrowband frequency spectra were obtained with a 1024-point FFT analysis and the average was calculated from 50 samples in each recording. Sonographic analysis of the signals, (previously digitised by a 16-bit acquisition card equipped with an antialiasing filter (low pass filter, fc=11.02 kHz; 120 dB/octave) at a sampling rate of 16 kHz), was conducted with the SYNTANA analytic package (Aubin, 1994; Lengagne et al., 2000).
Fig. 3. Sonogram of pellet noise impact during one hand pellet distribution (ca. 200 – 300 pellets).
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Fig. 4. Feeding sound spectrum of brown trout (—) compared to food-pellet sound spectrum recorded from the tank without fish (: : : ).
Fig. 5. Feeding sound spectrum of rainbow trout (—) compared to food-pellet sound spectrum recorded from the tank without fish (: : : ).
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3. Results 3.1. Description of the underwater ambient noise of culture systems Recorded during non-feeding periods, the background noise characteristics of the SEMII trout culture system were in two low frequency regions: one below 100 Hz, which peaked at 110 dB re 1 APa rms and the second around 400 Hz, which peaked at 92.8 dB re 1 APa rms (Fig. 1). Above 400 Hz, the sound level gradually decreased as the frequency increased and stabilized above 6 kHz at 50 –55 dB re 1 APa rms (Fig. 1, lower dashed spectrum). In the turbot culture system, underwater ambient noise was higher than in the trout culture system: 101 – 105 dB re 1 APa rms below 100 Hz and 96 dB re 1 APa rms around 375 Hz (Fig. 2, lower most dashed spectrum). Above 400 Hz, the ambient sound level decreased and stabilized at 65 dB re 1 APa rms between 7 and 10 kHz. 3.2. Description of the pellet sounds Noise from the impact of feed pellets on the water surface could interfere with feeding sounds (Fig. 1, upper spectrum). The highest energy distribution (in SPL, 83 93 dB re 1 APa rms) was measured in the frequency band between 1 and 2 kHz. Between 2 and 10
Fig. 6. Sonogram of feeding sound produced by brown trout. Note absence of feeding sounds before impact of pellets hitting water surface.
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kHz, the sound pressure level exceeded the underwater ambient noise level by at least 10 dB. The duration of this effect was between 200 and 600 ms (Fig. 3); the feed was distributed manually, and thus there may have been some variability in the number of feed pellets distributed each time and in their dispersion within the tank. 3.3. Description of the feeding sounds For both trout species, feeding activity starts as feed pellets hit the water surface but, within the 0 – 2 kHz frequency band, feeding sounds are masked by pellet impacts on the water surface (Figs. 4 and 5). For brown trout, feeding sounds are clearly distinguishable from ambient noise between 2.5 and 4 kHz (Fig. 4) and between 4 and 10 kHz, the acoustic energy decreases. The signal/noise ratio reached a maximum (about 15 dB) between 4 and 7 kHz. Sonograms (Fig. 6) confirmed the rapidity of the brown trout’s reaction to distributed feed: the average duration of feeding (including feed throw) was about 1400 ms, whereas the throwing periodicity was about 1800 ms. For rainbow trout (Fig. 5), the frequency band in which feeding activity can be clearly distinguished was from 2 to 5 kHz and the highest signal/noise ratio recorded was between 4 and 6 kHz (15 – 20 dB). Turbot feeding lasted longer than the trout. Pellet suctions take place after a few handfuls of pellets hit the water surface, thus representing the required time to stimulate
Fig. 7. Sonogram of feeding sound produced by the turbot. Suction feeding noises are observed before and after pellet impacts on water surface.
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Fig. 8. Comparison of feeding sound spectra of brown trout (: : : , lower spectrum), rainbow trout (: : :, medium spectrum), and turbot (—, upper spectrum) in farming environment.
fish feeding. Suctions intensified and then decreased over approximately one minute. After the stimulation period (ca. 4 – 5 s), the feeding process was continuous between two consecutive pellet distributions (Fig. 7). The sonogram and the narrow-band frequency spectra (Fig. 2) showed that turbot feeding noise is detected over a wide frequency band of up to 10 kHz or more. Between 3 and 9 kHz, the sound level reached 80– 90 dB re 1 APa rms and the corresponding signal/noise ratio was between 15 and 20 dB. Comparisons between the feeding noise spectra of these three fish species indicate that their frequency spectra are similar within the 2 –5 kHz frequency band (Fig. 8), but differ within the 7 – 9 kHz frequency band.
4. Discussion In aquaculture systems, low frequency noise (
J.P. Lagarde`re et al. / Aquaculture 240 (2004) 607–616
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higher frequency band, the two feeding strategies analysed (suction (turbot) and suction+ forward swimming (trout)) were easily identifiable. Under culture conditions, the feeding behaviours of the two trout species are different: rainbow trout pick up pellets at the water surface, whereas brown trout ingest pellets under the water surface. However, in spite of this difference, their feeding sounds are similar. For both trout species, the maximum feeding signal/noise ratio was observed between 4 and 6 kHz. This same frequency band is also observed in feeding and swimming noise studies of other species such as the: Atlantic horse mackerel (1.6 –4 kHz; Shishkova, 1958), Japanese horse mackerel (0.6 –8 kHz; Kaparang et al., 1999), yellowtail (4– 6 kHz; Takemura et al., 1988), and the yellowtail and amberjack (4– 8 kHz; Kaparang et al., 1998). For feeding turbot, the maximum signal/noise ratio observed was between 6 and 9 kHz at 15– 20 dB and was consistent with our previous results (Lagarde`re and Mallekh, 2000). The comparison between turbot and trout showed that frequency spectra were similar within the frequency band of 2 – 5 kHz. The 7– 9 kHz frequency band seems to be characteristic of feeding turbot and, furthermore of the exclusive suction feeding mode. This hypothesis is supported by the observations of Takemura et al. (1988) made during carp feeding behaviour study. In this species, which also uses an exclusive suction feeding mode, the high frequency band (4– 9 kHz) characterised feeding activity and showed a maximum acoustic energy between 7 and 9 kHz. Mallekh et al. (2003) indicated that the acoustic characteristics of feeding sounds may be potentially useful for controlling feed distribution in aquaculture. In turbot culture systems, this interest is not only due to the fact that acoustic energy varies over periods of more or less than 1 min depending on the variation in feeding intensity, but also to the nonalteration of the frequency band that characterises the turbot feeding sounds (7 –9 kHz) by environmental noises. The use of feeding sounds of active predators, such as trout, will be more difficult. First, the rapid pellet capture by these species superimposes feeding sounds and pellet impacts, in addition to noise related to variations in swimming speed and splashing. Nonetheless, a suitable signal could be used within the short time between consecutive feed distributions (ca. 1000 ms). Secondly, the frequency range limitation of the feeding sounds (20 –6000 Hz) presents some practical issues. The 20– 400 Hz frequency band is inappropriate for aquaculture applications since it is masked by the ambient noise of land based aquaculture systems (water flows, pumps, aerator, etc.) or to noise related to variation of atmospheric parameters in rearing conditions at sea (Wenz, 1962; Urick, 1983; Zakarauskas, 1986 ; Lagarde`re et al., 1994). The 4– 6 kHz frequency band offers the best opportunity for detection of feeding activity because it has a weak interference with the noise of land based aquaculture systems, however these frequencies could be masked by meteorological noise (rainfall, wind, etc.) in the outdoor ponds or enclosures.
Acknowledgements This study was financially supported by the ‘‘Cellule de Valorisation de la Recherche du CNRS’’ and the ‘‘Conseil Re´gional de Poitou-Charentes’’. We wish to thank J. Guarini for improving the language.
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