Oecologia (2008) 156:921–929 DOI 10.1007/s00442-008-1041-y
BEHAVIORAL ECOLOGY - ORIGINAL PAPER
Temporal patterns in ambient noise of biological origin from a shallow water temperate reef Craig A. Radford · Andrew G. JeVs · Chris T. Tindle · John C. Montgomery
Received: 4 December 2006 / Accepted: 26 March 2008 / Published online: 7 May 2008 © Springer-Verlag 2008
Abstract A systematic study of the ambient noise in the shallow coastal waters of north-eastern New Zealand shows large temporal variability in acoustic power levels between seasons, moon phase and the time of day. Ambient noise levels were highest during the new moon and the lowest during the full moon. Ambient noise levels were also signiWcantly higher during summer and lower during winter. Bandpass Wltering (700–2,000 Hz and 2–15 kHz), combined with snap counts and data from other studies show that the majority of the sound intensity increases could be attributed to two organisms: the sea urchin and the snapping shrimp. The increased intensity of biologically produced sound during dusk, new moon and summer could enhance the biological signature of a reef and transmit it further oVshore. Ambient noise generated from the coast, especially reefs, has been implicated as playing a role in guiding pelagic post-larval Wsh and crustaceans to settlement habitats. Determining a causal link between temporal increases in ambient noise and higher rates of settlement of reef Wsh and crustaceans would provide support for the importance of ambient underwater sound in guiding the settlement of these organisms. Keywords Larval settlement · Snapping shrimp · Sea urchins · Ambient underwater sound · Fish
Communicated by Roland Brandl. C. A. Radford (&) · A. G. JeVs · J. C. Montgomery Leigh Marine Laboratory, University of Auckland, PO Box 349, Warkworth, New Zealand e-mail:
[email protected] C. T. Tindle Physics Department, University of Auckland, PO Box 92019, Auckland, New Zealand
Introduction Many coastal invertebrates and Wsh produce planktonic larvae that undergo development in the waters over the continental shelf usually tens of kilometres away from coastal settlement sites. A critical period in the development of larvae is the migration from the continental shelf waters back to settlement sites on the coast. It had been thought that larval settlement was largely passive, driven by physical factors such as the prevailing hydrodynamic regime. It is now known that crab megalopae and spiny lobster pueruli (Shanks 1995; JeVs and Holland 2000; JeVs et al. 2005) and some Wsh larvae (Stobutzki and Bellwood 1994; Leis and Carson-Ewart 1997; Stobutzki 1997; Stobutzki and Bellwood 1997; Stobutzki 1998; Leis and Carson-Ewart 1999; Fisher and Bellwood 2003; Fisher et al. 2005) have surprisingly good swimming abilities. Furthermore, studies on juvenile reef Wsh show shoreward migration at night, implying an ability to orient to shore (Stobutzki and Bellwood 1998). Recent experimental evidence suggests that underwater sound can be used as an orientation cue by pelagic post-larval reef Wshes and crustaceans (Tolimieri et al. 2000; Leis et al. 2002; Tolimieri et al. 2002; JeVs et al. 2003; Leis and Carson-Ewart 2003; Leis et al. 2003; Simpson et al. 2004; Tolimieri et al. 2004; Simpson et al. 2005a; Montgomery et al. 2006; Radford et al. 2007). Underwater sound has the potential to act as a long-distance orientation cue because it travels with relatively little attenuation. Ambient sea noise is composed of frequencies from a combination of acoustic sources. Abiotic ambient background noise in the nearshore environment is largely the result of wind and waves that produce noise of frequencies in the range 10–1,000 Hz (Knudsen et al. 1948; Wenz 1962). Biotic sources of ambient noise are mammals, Wsh and crustaceans involved in reproductive
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displays, territorial defence, feeding or echolocation, and they cover a very wide range of frequencies (Knudsen et al. 1948; Tait 1962; Wenz 1962; Cato 1976, 1992, 1997b; McCauley and Cato 2000; Samuel et al. 2005). The physics of sound propagation and recordings of ambient sound provide some theoretical support for the potential of sound being used as an orientation cue (Montgomery et al. 2006). Electrophysiological studies provide evidence of the hearing competence of adults and to a lesser extent pre-settlement larvae, indicating that Wsh and crustaceans may have the sensory capability to use sound to Wnd reefs (Budelmann 1992; Popper and Fay 1993; Fay and Edds-Walton 1997; Popper et al. 2001; Simpson et al. 2005b; Wright et al. 2005). Furthermore, behavioural experiments have provided some direct evidence that sound is used by these animals to guide their movements. The Wrst behavioral experiment replayed recorded reef sound in the vicinity of light traps, which were moored in a bay some distance away from any reefs (Tolimieri et al. 2000). The light traps associated with the replayed reef sound (180 dB re 1 Pa at 1 m) had signiWcantly higher catch rates of the pelagic larvae of triple-Wn reef Wsh compared to silent control traps. Two subsequent studies have repeated the experiment and demonstrated the same phenomenon for a wide range of tropical reef Wsh species (Leis et al. 2003; Simpson et al. 2004). The same methods have shown that the phenomenon also occurs for some decapod larvae in temperate waters (JeVs et al. 2003). Further experiments using choice chambers have shown that late-stage larval Wsh and decapods orient to sound in a manner that is consistent with guiding their movement toward reefs as suitable settlement habitat (Tolimieri et al. 2002, 2004; Radford et al. 2007). Simpson et al. (2005a) were able to show that artiWcial patch reefs constructed of dead coral had higher levels of settlement of many species of reef Wshes when they were associated with replayed reef sounds compared to patch reefs without sound. Despite the potential importance of ambient underwater sound in the orientation and recruitment of a wide range of key reef species relatively little is known about what features of underwater noise in shallow coastal waters are likely to be useful for orientation. In particular, temporal variability in the power and spectra of ambient noise has the potential to greatly inXuence its usefulness for guiding the orientation of larvae that are located oVshore of coastal reefs. A daily pattern in ambient noise has been observed at two locations in New Zealand (Tait 1962; Castle 1974) and in some places around temperate and tropical Australia (Cato 1976, 1978, 1980, 1992, 1997a). Evening and morning choruses, consisting of a marked increase in biotic noise have also been identiWed as a common feature of a number of coastal environments (Tait 1962, Breder 1968; Cato 1978). Predictable temporal variability (time of day,
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daily, lunar phase, seasonal) will largely be of biotic origin. Therefore, the aim of this study was to examine the temporal periodicity of ambient noise levels from a coastal location in north-eastern New Zealand, and to determine the biological sources of this noise.
Materials and methods To assess temporal periodicity in ambient noise at North Reef, Leigh (36°15⬘45⬙S, 174°47⬘33⬙E) north-eastern New Zealand, we recorded ambient noise over two moon phases (new moon and full moon where moon phase was considered to be 3 days either side of the astronomical event) and over the four austral seasons, summer (December–February), autumn (March–May), winter (June–August), and spring (September–October). For each season the sampling was undertaken towards the middle and end of the season to eliminate water temperature lag issues. A recording hydrophone was placed 1 m oV the seaXoor in 21–23 m of water depending on the tide, and 80 m away from the margin of the coastal fringing reef, and consisted of a calibrated Sonatech BM 216 omnidirectional hydrophone (10 Hz–60 kHz Xat response) connected to an automated recording system contained in an underwater housing. The system had a Unidata Micrologger timing and relay unit operating a Sony TCD-D8 digital recorder with a sampling rate of 48 kHz which took a 5-min recording every hour, on the hour. The hydrophone was calibrated by recording a NetMark 1000 acoustic pinger (speciWcations: source level 130 dB re 1 Pa at 1 m, 10 kHz signal, 300 ms pulse length, 4 s repetition rate). The recordings were transferred to a PC and analysed using Matlab software with codes speciWcally written for these recordings. Wind speed and direction data were recorded simultaneously every hour at the climate station at the nearby Leigh Marine Laboratory.
Data analysis To determine if variability in wind speeds might exert an inXuence on the abiotic component of ambient underwater sound recordings, the hourly wind speeds (which are an average of wind speeds recorded every 2 s during that hour) for the duration of the sampling period for each of the diVerent temporal sampling events were compared using ANOVA. Each 5-min sound recording was divided into 10-s subsamples within which Wve were randomly selected, then bandpass Wltered for 700–2,000 Hz and 2–15 kHz frequency bands to calculate measured levels (ML) for each. For each of the Wve randomly selected sub-samples the number of snaps produced by snapping shrimp was also
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estimated. This was achieved by setting a threshold level on the raw data and any transient spike that was less than 0.2 s above the threshold was counted as a snap by a shrimp. Time of day was divided into four periods; night, dawn, day and dusk. The periods were deWned based on light data obtained from light measurements taken at the nearby climate station at the Leigh Marine Laboratory. Night was deWned as having no light (0 MJ m2 h1); dawn and dusk were deWned as having less than 1.2 MJ m2 h1 of light; and day as having greater than 1.2 MJ m2 h1 of light. For each period the ML for the frequency bands and number of snaps were averaged and analysed using a general linear mixed model, with weighted means. Covariance parameter estimates were calculated for the auto-regressive error structure ARH(1), to account for the repeated nested factor [Day(Moon Phase £ Season)]. These analyses enabled comparisons in the mean ML data and the number of snaps to be made among Time of Day, Moon Phase and Season. SigniWcant diVerences between individual pairs of means were determined using Tukey’s tests. All data were analysed using SAS software and presented as the statistical mean § SEM. Power spectra were generated using fast Fourier transformation analysis of the randomly selected 10-s samples, which were smoothed with an 11-point triangular window. Data were high pass Wltered to 100 Hz to remove any hydrostatic eVect of surface waves and any 50-Hz interference. In addition, ambient sound below 100 Hz tends to have a large component of abiotic noise and therefore was not of speciWc interest to this study (Knudson et al. 1948; Wenz 1962).
Results Wind speeds were similar between both Moon Phase (F1,190 = 0.27, P = 0.6), among Seasons (F3,188 = 1.21, P = 0.7), and the interaction (Moon Phase £ Seasons) (F3,181 = 0.81, P = 0.1). Therefore, wind was eliminated as the cause of any diVerences in the intensity and power levels of the recorded ambient sound.
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700–2,000 Hz from noon to dusk compared to the other three seasons. During the full moon, autumn and spring had the greatest rise (15 dB re 1 Pa2/Hz) from noon to dusk in the frequency band 700–2,000 Hz. The diVerence between the noon and dusk power spectra is at its minimum during winter for both moon phases. New moon dusk periods during all the seasons were consistently more intense (> 8 dB re 1 Pa2/Hz) than the full moon periods within the same season. Frequency band 700–2,000 Hz The intensity levels of ambient underwater noise in the 700–2,000 Hz bandwidth (Fig. 2) varied signiWcantly among Seasons (F3,121 = 145.5, P < 0.0001), Moon Phase (F1,121 = 150.4, P < 0.0001), and Time of Day (F3,3 = 22.8.7, P < 0.05). There was also a signiWcant interaction between the factors Seasons £ Moon Phase (F3,121 = 16.5, P < 0.01). However, the other interactions were not signiWcant: Seasons £ Time of Day (F6,3 = 0.4, P = 0.88), Moon Phase £ Time of Day (F3,3 = 0.2, P = 0.81) and Seasons £ Moon Phase £ Time of Day (F6,3, = 1.2, P = 0.66). The highest sound intensity was at dusk on the new moon during summer (143 § 1 dB re 1 Pa), which was signiWcantly higher than the new and full moon periods both during winter and spring. The lowest sound intensity was during the day in the full moon phase in winter (88 § 1 dB re 1 Pa). For summer, winter and spring the new moon periods had signiWcantly higher sound intensity than their respective full moon periods. The diVerence in intensity between the new moon and full moon within a season was greatest in summer (30 dB re 1 Pa) with a signiWcant reduction in the diVerence during winter (3 dB re 1 Pa). Dusk periods in summer, winter and spring were consistently the time of the day with the highest sound intensity, followed by dawn, night and day, with a signiWcant decrease in intensity between each. Overall, for this frequency band, summer was the time of the year with the highest sound intensity, which was signiWcantly more intense than during winter and spring. Frequency band 2–15 kHz
Choruses Power spectra analysis shows that in all seasons and during both moon phases there was a rise in the frequency 700– 2,000 Hz bandwidth during dusk compared to noon (Fig. 1). This generally had a peak power level between 1,000 and 1,600 Hz. There was also a less pronounced rise in the spectra between 2 and 7 kHz which generally had a peak power level at around 2,500 Hz. The new moon phase in summer was observed to have the greatest rise (20 dB re 1 Pa2/Hz) in overall power level for the frequency band
Intensity levels of ambient underwater noise in the 2–15 kHz bandwidth (Fig. 3) varied signiWcantly among Seasons (F2,121 = 108.5, P < 0.0001), Moon Phase (F1,121 = 150.4, P < 0.0001), and Time of Day (F3,3 = 58.7, P < 0.01). There was also a signiWcant interaction between the factors Seasons £ Moon Phase (F2,121 = 12.6, P < 0.01). Overall, the 2–15 kHz frequency bandwidth exhibited the same patterns as the 700–2,000 Hz bandwidth. The sound intensity in this frequency band was greatest at dusk during the new moon in summer
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Fig. 1 Power spectra of the noon and dusk periods (dB re 1 Pa2/Hz) for North Reef for a summer—new moon; b autumn—new moon; c winter—new moon; d spring—new moon; e summer—full moon; f autumn—full moon; g winter—full moon; h spring—full moon
(134 § 1 dB re 1 Pa) with the quietest time of the year being during the day in winter on the full moon (86 § 1 dB re 1 Pa). The diVerence in intensity between the new moon and full moon within a season was greatest in summer (34 dB re 1 Pa) with a signiWcant reduction in the diVerence during winter (4 dB re 1 Pa).
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Snapping shrimp The number of snaps produced by snapping shrimp (Fig. 4) exhibited signiWcant diVerences for the Time of Day (F3,8 = 62.4, P < 0.001), Moon Phase (F1,8 = 112.9, P < 0.001) and Seasons (F3,8 = 81.6, P < 0.001). Snapping
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Fig. 2 Measured levels (dB re 1 Pa) of the 700–2,000 Hz frequency for North Reef during the new and full moon for a summer; b autumn; c winter; d spring. Filled circle New moon, open circle full moon
Fig. 3 Measured levels (dB re 1 Pa) of the 2–15 kHz frequency band for North Reef during the new and full moon for a summer; b autumn; c winter; d spring. Filled circle New moon, open circle full moon
shrimp produced signiWcantly more snaps during dusk than any other time of the day, and more snaps during the new moon compared to the full moon. In winter, there were signiWcantly fewer snaps produced compared to the other three
seasons. All the interactions also exhibited signiWcant diVerences, Seasons £ Moon Phase (F3,8 = 28.8, P < 0.001), Moon Phase £ Time of Day (F3,24 = 32.3, P < 0.001), Seasons £ Time of Day (F9,24 = 16.2, P < 0.001) and Seasons £ Moon Phase £ Time of Day (F9,24 = 5.0,
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P < 0.001). Snapping shrimp produced signiWcantly more snaps in summer during dusk on the new moon than in any other season and moon phase (Fig. 4). The dusk periods during summer, autumn and spring for the new moon (3,134 § 747 snaps/10 s; 859 § 764 snaps/10 s; 909 § 776 snaps/10 s, respectively) and full moon (579 § 378 snaps/ 10 s; 8 § 6 snaps/10 s; 12 § 5 snaps/10 s, respectively) had signiWcantly more snaps compared to night, dawn and day periods. However, the number of snaps during dusk for both the moon phases was similar in winter, but was signiWcantly higher at night compared to day in winter.
Discussion Ambient underwater noise at North Reef, north-eastern New Zealand, shows signiWcant diurnal, lunar, and seasonal periodicity. There was a very consistent rise in power levels in the bandwidths 700–2,000 Hz and 2–7 kHz from noon to dusk (evening chorus) often by as much as 20 dB re 1 Pa2/ Hz. Intensity levels in these frequency bandwidths varied over 24 h, the day is the quietest time followed by night, then dawn, with dusk being the noisiest. Over the lunar month, reef noise during the new moon period is signiWcantly more intense than during the full moon period, often by up to 30 dB re 1 Pa2/Hz. Seasonality also signiWcantly aVects the power of ambient noise, which is signiWcantly more intense in summer than in autumn, winter and spring. Snapping shrimp were an important source of biotic sound and exhibited signiWcant diurnal, lunar and seasonal periodicity in their sound production. There were signiWcantly more snaps produced during dusk compared to day, night and dawn. The new moon had signiWcantly more snaps compared to the full moon. Seasonally, there were signiWcantly greater numbers of snaps (»10 times more depending on the time of day and moon phase) produced during summer than any other season. The term “evening chorus” is used to describe the combined ambient noise produced when large numbers of individual crepuscular animals are producing sounds during dusk and early night. In the present study evening choruses were observed in every 24-h observation period during all the seasons. The only other detailed study of this kind was conducted by Breder (1968) in the tropical setting of Lemon Bay, Florida. Breder (1968) showed that the Wsh Galeichthys felis and Opsanus beta produced more intense evening choruses during summer than winter and on the new moon compared to the full moon. A number of studies on ambient underwater noise around Australia have shown the presence of choruses (Cato 1978, 1992). The choruses were observed in the frequency band of approximately 400 Hz to approximately 5 kHz and lasted for a few hours.
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Fig. 4 Mean number of snaps of snapping shrimps in 10 s for North Reef during the new and full moon for a summer; b autumn; c winter; d spring. Filled circle New moon, open circle full moon. Note diVerent ordinate scales
The most consistent time of occurrence was immediately after sunset, although some choruses were observed immediately before sunrise. The bandwidth of the choruses
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reported in this present research were of a much lower frequency range, 700–2,000 Hz, which could possibly be due to the smaller number of noise-producing organisms, especially Wsh, in New Zealand’s temperate waters compared to the tropical waters of Australia where Cato (1976, 1978, 1992) conducted his research. The noise increase for evening choruses above daytime ambient levels is on average about 20 dB for North Reef, New Zealand, during summer. This is consistent with Australian choruses where Cato (1992) observed on average an increase of 20 dB during the evening chorus over daytime sound levels. Early research in New Zealand tentatively identiWed the source of the evening chorus in the frequency band 700– 2,000 Hz to be the sea urchin Evechinus chloroticus (Castle 1974; Castle and Kibblewhite 1975). Castle (1974) suggested the urchin test could act as a Helmholtz resonator that would be capable of amplifying feeding noises produced by individual urchins. Radford et al. (2008) have conWrmed this with laboratory recordings of urchin feeding behaviour. Urchins are nocturnally active animals (Nelson and Vance 1979; Jones and Andrew 1990; Hereu 2005) that are preyed upon by nocturnal and diurnal predators. It is possible that the smaller increase in the power level observed during the evening chorus on the full moon compared to the new moon was due to the small urchins remaining in their crevices during the full moon because they become more susceptible to visual predators. The most ubiquitous biological component of ambient noise is the snapping shrimp, since it is evident throughout the world in shallow, warm waters, usually in depths of less than 60 m and latitudes less than about 40° (Knudsen et al. 1948; Everest et al. 1948; Fish 1964). The shrimp responsible belong to the genera Alpheus spp. and Synalpheus spp. (Fish 1964). Large numbers of shrimp can produce a sizzling or crackling sound, in the frequency range 2–12 kHz, a characteristic seen in shallow waters around both Australia (Cato 1976, 1978, 1992, 1997a) and New Zealand. The present research showed that snapping shrimp form a large part of the elevated levels of noise during dusk, dawn and night, with the intensity and power levels in the frequency range 2–15 kHz increasing above that of the ambient background noise. The noise in this bandwidth was signiWcantly more intense in the summer compared to winter by 25 dB re 1 Pa on average. Patterns in the numbers of snaps produced by these animals are consistent with the changes in overall ambient intensity levels. This increase in snapping could be a result of increased activity whilst the water is warmest during summer because these animals are poikilotherms. Also, because there is less predation pressure under darker conditions, the shrimp are likely to be more active during periods with both warmer water temperatures and low light (i.e. new moon during summer). As the water cools progressively following summer, the activity levels of
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snapping shrimp probably decrease consistent with the decreased abundance of snapping observed in this study. Source levels of a single snap by a snapping shrimp can be as high as 190–210 dB re 1 Pa2 at 1 m (peak to peak) in the frequency range 2–15 kHz (Everest et al. 1948; Au and Banks 1998; Versluis et al. 2000). Consequently, as snapping shrimp can occur in large numbers on the seaXoor, they will most often be the dominant biological source of noise in the frequency band of 2–15 kHz. The present study has shown that a large component of the transient noise produced on the reef is the 700– 2,000 Hz frequency range produced by E. chloroticus (Radford et al. 2008). This component is within the most sensitive range (100–3,000 Hz) of hearing of generalist Wsh and crustaceans (Budelmann 1992; Myrberg 1996; Kenyon et al. 1998; Popper et al. 2001). It has also shown that there was marked temporal variability in the intensity of the sound produced within this range, with the highest intensities produced on the new moon in summer and the lowest on the full moon in winter. These periods of highest sound production are correlated with the temporal variation in larval Wsh settlement in tropical and temperate reef systems, with the greatest larval settlement generally occurring around the time of the new moon during summer (Robertson et al. 1988; Victor 1991; Milicich 1986; Kingsford 1992; Tricklebank et al. 1992; Thorrold et al. 1994; Caselle and Warner 1996; Dufour et al. 1996; Sponaugle and Cowen 1996; Lozano and Zapata 2003; McIlwain 2003). Controlled play-back experiments at a range of intensities could be used to test the hypothesis that there is a proximate causal link between temporal increases in ambient noise and higher rates of settlement of reef Wsh and crustaceans. Any such causal link would provide further support for the importance of ambient underwater sound in guiding the settlement of these organisms. Acknowledgements We would like to thank Nick Tolimieri and Brian McArdle for invaluable advice about statistical analysis of these data and Andy Heap for technical help with the temporal recorder. Anonymous referees helped to improve this manuscript. This research was supported by the Marsden Fund of the Royal Society of New Zealand.
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