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Synchronous behaviour of cetaceans observed with active acoustics
Deep-Sea Research II 98 (2013) 445–451
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Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2
Synchronous behaviour of cetaceans observed with active acoustics Olav Rune Godø a,n, Lise Doksæter Sivle a, Ruben Patel b, Terje Torkelsen c a b c
Institute of Marine Research, P.P. Box 1870, 5817 Bergen, Norway CodeLab Bergen, Klostergaten 26, 5005 Bergen, Norway METAS, Nedre Åstveit 12, 5106 Bergen, Norway
art ic l e i nf o
a b s t r a c t
Available online 29 June 2013
Scientific split-beam echosounders are sensitive instruments for observing biomass densities and individual behaviour. Earlier studies have demonstrated that these instruments can be used to study diving behaviour of cetaceans. In this paper, we go into more detail about the recorded signal to see if and how acoustic split-beam data can be used to extract information about synchronous behaviour and other species related characteristics. Data of several cetacean individuals were collected by a moored echosounder pinging upwards from about 900 m in the Charlie Gibbs Fracture Zone. In this paper, we discuss methodological issues associated with using split-beam tracking of large marine animals. Further we demonstrate that target tracking of cetaceans can be used to study solo dives as well as behavioural synchrony. We also show that paired signals can easily be interpreted as false synchrony due to the size of the animals. In such cases a rough estimate of the diameter, and hence size, of the animals can be estimated. We emphasise on four examples that clarify methodological challenges including synchronous swimmers as well as large single cetaceans that might be interpreted as two synchronous swimmers. The applied technology requires that the animals remain in a narrow acoustic beam for long enough time to extract behavioural information. The technology can be improved by developing automatic tracking of cetaceans with a steerable transducer. This will substantially increase the search volume and enable tracking of cetaceans over longer periods and thus, produce more realistic information about the whale behaviour. & 2013 Elsevier Ltd. All rights reserved.
Keywords: Whale behaviour Synchrony Active acoustics Tracking Feeding
1. Introduction Synchronous movements are common features in terrestrial and marine social animals (Engel and Lamprecht, 1997; Conradt and Roper, 2000). Whereas such behavioural characteristics often are associated to anti-predator tactics it might also be an efficient hunting and teaching strategy (Senigaglia and Whitehead, 2012; Senigaglia et al., 2012; Tremblay and Cherel, 1999). Synchrony feeding may ease energetic cost due to hydrodynamic advantages and has particularly been observed in mother–calf pairs (Noren and Edwards, 2011; Tyson et al., 2012). Qualitative and quantitative studies of synchronous behaviour on land can be done with simple visual methods, but similar results from underwater realm have been inferred from indirect method like tagging (Tremblay and Cherel, 1999; Tyson et al., 2012) or from visual observation at surface (Senigaglia and Whitehead, 2012).
n
Corresponding author. E-mail addresses: [email protected] (O.R. Godø), [email protected] (L.D. Sivle), [email protected] (R. Patel), [email protected] (T. Torkelsen). 0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.06.013
Direct observation of detailed behavioural patterns of individual marine fishes has been enabled by tagging (Metcalfe and Arnold, 1997) and by split-beam acoustic target tracking techniques (Handegard, 2007; Kaartvedt et al., 2009). Active acoustics has also been used to observe marine mammals (Doksæter et al., 2009) as well as birds (Benoit-Bird et al., 2011). Acoustic split-beam echosounder techniques (Brede et al., 1990; Ona, 1999; Foote, 1987) allow three dimensional positioning of individuals in the beam volume. Distances to target from the four sectors of the split-beam transducer are estimated from the differences in the phase angle (time delay) of the backscattered signal as observed at these four sectors (see Supplementary video). These distances are used to triangulate the target position in the beam. Behavioural characteristics of fish movement in time and space have been developed using target tracking techniques (Handegard et al., 2005). The pulse (1 ms about 1.5 m) travels through the acoustic beam and when several individuals are present in the same pulse volume the phase angle will show high variability across samples and hence undefined position. When observing samples with integrity (co-variation) in the phase information of the backscattering signal it can be defined as a valid target. The target tracking algorithm then allocates accepted
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targets to specific individuals, thus, allowing their trajectories to be drawn. High ping to ping variation is often caused by multiple individuals simultaneously present in the same pulse volume. Integrity, i.e. smooth ping to ping changes of the phase angles, is interpreted as consistency in target movement, as expected for the swimming trajectory of a fish. Supplementary material related to this article can be found online at http://dx.doi.org/10.1016/j.dsr2.2013.06.013. This paper focuses on the methodology employed in four studies on diving animals with different behavioural characteristics. Our aim is to demonstrate that active acoustic split-beam technology can be used to study detailed individual and synchronous behaviour of top predators in the marine environment and to report unique behavioural recordings of whales apparently foraging over the mid-Atlantic ridge. The method allows the observation of animals and records fine scale behavioural characteristics such as feeding to the full depth of diving capabilities without prior selection and tagging process.
2. Materials and methods In this paper, the targets are tracked manually and the tracks are used to study whale behaviour. Systematic changes in acoustic backscattering strength of tracked fish enable the characterisation of fine details like tail beat frequency of single fish (Handegard et al., 2009). We use tracked targets to study further the data presented by Doksæter et al. (2009) to extract details about behaviour of diving cetaceans with particular emphasis on dives of multiple individuals. Dives were studied in detail to extract quantitative information on synchronous movement patterns. Data were collected with a moored split-beam echosounder launched on July 22, 2004, at N51131.6′ and W030119.9′ at a bottom depth of 920 m. The water column from 910 m to surface (Fig. 1) was observed during a period of 10 months until end of May 2005 (Wenneck et al., 2008). The observation frequency and angle were 38 kHz and 71, respectively, and the ping rate was 30 min 1. Thus, the footprint diameter of the acoustic beam at surface was 110 m and gradually reduced to about 100 m at 100 m depth, which includes the depth range of all dives in our data set (Table 1). Since the animals swam in and out of the beam at various depths, the observation time of the individual targets varied a lot. Only acoustic targets (cetaceans) satisfying certain criteria were included in the analysis (see Table 2), but their identity cannot be established from this analysis. The target tracking principle supported by the split-beam transducers utilises the ability of the transducer to record the echoes separately at four quadrants of the transducer. The
principle geometry is illustrated in Fig. 2 and accordingly, the arrival angle (θ) can be calculated θ ¼ sin 1 ðΔr=dÞ The difference in range between arrivals at the two transducer quadrants can be calculated using the arrival time delay or based on the phase shift of the signal at arrival. This is a far field approximation which is valid for all targets analysed in this paper. The selected acoustic targets, likely to represent one or more cetaceans, in our analysis (see Table 1) are classified under Category 1 (the best) by Doksæter et al. (2009). The analysis includes three consecutive processes:
Visual interpretation: Splitting observations into lone-divers (single
individuals) and multiple-divers (more than one animal). In some instances, both types of echoes were included in the same dive and in such cases they were separated and identified as single- and multi-phases, where single-phase includes one animal and multiphase includes two or more (see Figs. 3 and S1–S12). Quantitative interpretation: We studied the echoes from lonedivers and single-phase divers further to distinguish between single targets when they satisfy criteria as described by Handegard et al. (2009) and multiple targets if not satisfying these criteria (see the previous paragraph). Tracks were isolated manually in the echogram (see Fig. 3). Then a target detector was applied to each of the isolated regions to extract valid targets using the settings given in Table 2. In some instances two detections were observed in one ping inside one region. The position data from these detections were averaged. Quantitative assessment of synchronous behaviour: Finally, based on the available accepted single target measurements, we evaluated synchrony in whale behaviour for multiple-divers and multi-phase divers based on the similarity in behaviour of neighbouring animals. In our case, the observed phase angles are converted to distances from the centre of the beam, and correlation between the estimated distances over time is used to evaluate synchrony. These distances also allow the study of impact of proximity on synchrony.
3. Results Cetaceans were repeatedly observed diving from the surface to acoustic layers at 50–100 m comprising mesopelagic fish such as Muller’s pearlside (Maurolicus mulleri) (Opdal et al., 2008), during the time series. Along with dives to well-defined acoustic layers of
Fig. 1. A sketch of the acoustic buoy located at 910 m depth pointing upward (left panel). Right panel shows a zoomed echogram from surface to 200 m. There are three whale dives (A, B, and C) at the echogram appearing as clear green/cyan (grey) vertical moving lines. The maximum diving depth is 75 m.
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Table 1 Overview of the analysed targets (see also Figs. S1–S12). Duration refers to the longest track when multiple targets are present in the figures. Lone and synchronous refer to the number of dives defined as lone dives and synchronous dives. NA, not applicable. Date
Obs. number
Time (UTC)
Duration (min)
Max diving depth (m)
Number of animals
Figure
Lone
Synchronous
10.08.2004 05.09.2004 05.09.2004 21.09.2004 03.11.2004 03.11.2004 26.11.2004 27.11.2004 27.11.2004 16.12.2004 18.02.2005 10.03.2005 Sum
Obs. 1 Obs. 5 Obs. 70 Obs. 11 Obs. 17 Obs. 45 Obs. 59 Obs. 2 Obs. 3 Obs. 62 Obs. 9 Obs. 68
16:05 18:19 19:29 17:54 00:23 03:02 13:14 00:21 04:51 04:02 11:28 08:36
2 2 2 3 4 2 1 2 2 6 3 2
72 14 44/85 19 71 14 26 30 55 60 16 18
3a 2 3 3 6 2 2 2 3 3 3 2
S1 S1 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12
2 1 3 3 NA NA NA NA NA 1 1 NA 11
1 NA 1 NA 3 1 1 1 1 1 1 1 12
a
It is four animals if track C is accepted as a multi-phase (see text).
Table 2 Settings for the single target detection in Large Scale Survey System software. TS is acoustic target strength. Variable (LSSS)
Setting
Explanation
MinTS MaxTS PulsLengthDeterminationLevel MinEchoLength MaxEchoLength MaxGainCompensation
30 10 5 0 3.8 10
Minimum TS value to be detected (dB) Maximum TS value to be detected (dB) Pulse length determination level (dB) Minimum echo length relative to pulse length Maximum echo length relative to pulse length Maximum gain compensation (dB)
Fig. 2. Illustration of the geometry of the received echo and how this can be used to estimate position of the target. The arrival angel of an acoustic signal arriving at two transducer quadrants is represented by two lines. θ represents the arrival angle which can be estimated based on the range difference (Δr) and distance between the transducer quadrants (d).
potential food, some shallow dives of individuals and groups that were probably travelling over the location (Figs. S1–S12) were also recorded. In this paper, we gave particular attention to few of the deeper dives, however, some key data and visual interpretation are associated with echograms of additional tracks (see Table 1 and Figs. S1–S12). A visual survey of the area was conducted in July 2004, and the species observed in the area around Charlie Gibbs Fracture Zone is shown in Table 3. 3.1. Visual interpretation Some details about the tracks given particular attention in this paper are summarised in Table 1 (Obs. numbers 1, 3, 17, and 59).
The tracks we interpreted and classified in accordance with the three categories are described in Section 2 (lone-divers, singleand multi-phases) (see also Figs. 3 and 4). The analysis under Section 3.2 follows this classification. The three dives in Fig. 3 are the same as indicated in Fig. 1 but observed with a different resolution. While A and B apparently are lone-divers, C looks like a lone diver during the start but the later split indicates that this is a multi-phase dive changing to two single-phase dives. Based on a ping to ping study of the tracks, we separated the tracks or part of tracks by red boxes as indicated in Fig. 3, lower panel. Similar categorisation is illustrated for Obs. numbers 17 (Fig. S6 track C) and 59 (Fig. S8) and extracted splitbeam data were used for the further analysis. Fig. 4, upper panel, shows a lone diver splitting into two and later three separate tracks. Panels A and B present variation in the phase angles and demonstrate that these angles stand out from the normal variability and thus, indicate that these tracks represent individuals swimming close together. 3.2. Quantitative interpretation The visual interpretations in Section 3.1 illustrate that the echogram does not necessarily reflect the truth about the number of animals; both two and three animals emerged from what appeared to be a single individual. It should be kept in mind that the echogram separates animals only in the vertical direction. Vertically resolved individuals could be separated by large horizontal distances as the footprint of the acoustic beam is on the order of 100 m in diameter at the observation depth. Thus, animals that appear visually close are not necessarily synchronous swimmers. Furthermore, the visually interpreted lone-divers could theoretically be composed of more than one animal well separated horizontally in the beam but included in the same pulse volume when at similar depth. The target tracking approach may solve these issues. Such tracking must be done with settings adjusted to the observation situation, and the settings in Table 2 have been
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Fig. 3. Upper panel: echogram of Obs. number 1. This observation consists of three separate tracks: A, B and C. A and B are typical lone-divers, while C appears like a lone diver during the start when swimming through a layer of prey. The lone diver apparently split into synchronously swimming single-phase divers during ascent to the surface. Thus, the first part of the track is a multi-phase dive, while the second part is two single-phases. Lower panel: details of track C. T1 is the multi-phase when two cetaceans are swimming together in a prey layer. T2 and T3 are the single-phases, when the two animals separate and ascent towards the surface in a synchronous manner. Red (grey) boxes show the separated track, and black marks indicate identified accepted single target tracks as defined in LSSS (Table 2).
Table 3 Visual observations of marine mammals from the RV G.O. Sars at the Charlie Gibbs Fracture Zone in the area of the moored echosounder on Leg 1 of the Mar-Eco cruise (Wenneck et al., 2008) 17–18 June 2004. Common name
Scientific name
Minke whale
Balaenoptera acutorostrata Baleanoptera borealis Balaenoptera physalus Globicephala melas Lagenorhynchus acutus Mesoplodon sp. Physeter macrocephalus Balaenopetera sp.
Sei whale Fin whale Pilot whale White-sided dolphins Beaked whale Sperm whale Unidentified baleen whale
Total number
Number of observations
1
1
44 3
31 3
46 30
3 2
3 12
3 8
5
5
demonstrated to perform well in the current situation. For example tracking of large animals (45 m) such as cetaceans requires a higher setting of echo length and acoustic target strength due to their size. The proportion of the signals accepted as single targets is important for the evaluation and so is the stability of recorded single target information that is used to assess the absolute position of cetaceans in relation to each other. As seen in Fig. 3, a high portion of the pings are accepted by the tracker as single target, but not all. Concerning stability of the target information, we see that the phase angles (both directions) of the tracks, appearing from the grey scale in Fig. 4, stand out from the phase angles of the rest of the pixels in the echogram with respect to the stability and consistency. This indicates coordinated movements of individuals that are close to each other. Similar information is available for all dives.
3.3. Quantitative assessment The information extracted in Section 3.2 was used to assess the exact position of the targets with respect to the depth and position in the beam (phase angles of the signal). Obs. number 1 (Fig. 3) was split into single-phase and multi-phase tracks and the position in the beam estimated (Fig. 5). The very smooth parallel movements of the single-phase observations indicate parallel swimming animals with a distance of about 2–3 m. The quality of the positioning of the track is also confirmed by high correlation between x and y distances (converted from phase angles) (Table 4). Similar calculations are available for the Obs. numbers 17 and 58. The tracks of Obs. number 17 are more than 10 m apart vertically (Fig. 6) and the x and y distances are highly correlated (simple linear regression, Table 4), although r2 is lower than for Obs. number 1. The animals of Obs. number 58 are relatively close together vertically (2–4 m) but are separated horizontally by as much as 20–40 m (Fig. 7). Distances from the beam centre are loosely correlated in the x-direction but strongly correlated in the y-direction. In Table 1, we have given our interpretation of number of animals included in the studied examples (Figs. S1–S12) and number of dives defined as lone and synchronous dives. Based on our material it is indicated that about half of the dives are synchronous.
4. Discussion Our results demonstrate that a target tracking technique can be used to study diving behaviour of cetaceans and synchronous movements. The interaction between visual interpretation of the echograms and statistical analysis of the target information enabled the quantification of behaviour and interaction. We can see how individuals behave in relation to each other and this might have a range of applications with respect to the
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Fig. 4. Upper panel: echogram of Obs. number 3 showing three animals diving in synchrony. During the first part of decent the animals are inseparable. Then apparently three single-phase dives emerge. One of the animals separates from the two others, which continue to move close together from a depth of ∼20 m, thus, becoming a multiphase. Lower panel shows the phase angles where the diving whale stands out with consistent changes.
Table 4 Consistency in the variation of distance from centre (equivalent to phase angle) of Obs. numbers 1, 17 and 59 given as the correlation coefficient (r2) of the linear regression between comparable angles.
Fig. 5. Obs. number 1 with multi- (circles) and single-phase tracks (pyramid and cubes) showing the movements in the beam from 70 m to surface. Axis values are in metres. Range refers to surface as zero while x and y refer to centre of beam as zero.
understanding of individual and group behaviours in relation feeding, social behaviour, learning, etc. In our study, we used an active echosounder system operating at 38 kHz. This is within the hearing range of many cetaceans and thus, we cannot exclude the possibility that the acoustic system influenced the target behaviour. For example, our system received several instances of pulses of sound (noise) that could be whale vocalisations imitating the echosounder (see Fig. S5). Whale imitation of sounds, also anthropogenic, is a part of their learning and habituation process (Tyack, 2008), and low
Obs. number
X (m)
Y (m)
Number of parallel observations
1 17 59
0.96 0.82 0.10
0.90 0.79 0.96
18 9 9
power echosounder pulses have over time likely become part of the normal soundscape of marine animals, including cetaceans. It has e.g. been demonstrated that scientific sonars and echosounders do not affect the behaviour of killer whales (Knudsen et al., 2008), and the behavioural impact of the echosounder is, thus, considered low or negligible. The use of acoustic target tracking as a means of species or group identification requires some kind of validation. This could be a visual observation at surface or passive acoustic recording systems that identify animals through their vocalisation (see e.g. Erbe and King, 2008; Andre et al., 2011). During a survey along the mid-Atlantic ridge in summer of 2004 (www.mar-eco.no), several species of cetaceans were found to occupy the Charlie Gibbs Fracture Zone (Table 3). The lack of any kind of positive confirmations, such as simultaneous visual observations together with the novelty of the method, makes any attempts to verify the cetacean species of the recordings presented in this study highly speculative. However, based on the list of occurring species in Table 3, together with dive depth, shape of the track and the observed number of animals, we may do some speculations. Diving depth of the tracks varies from 14 to 85 m and is within the diving range of all the species represented in Table 3. Some of the tracks show diving towards and into distinct prey layers e.g.
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Fig. 6. Time (observation number)–depth plot of the track information of Obs. number 17. Double arrow line indicates a range of 10 m.
Fig. 8. Autonomous target follower based on a moving transducer (T) directing a searching beam (B) either systematically through a searching pyramid (opening angle of 601) or actively following a specific target over time. The searching volume increases with range (h) and at 500 m range sides in the searched rectangle (a and b) will be more than 800 m.
Fig. 7. Distances from centre of beam of the single-phase tracks of Obs. number 59. Double arrow line indicates a range of 30 m.
tracks A and C in Fig. 1, which have a dive with a U signature, with the dive ending just underneath a prey layer, which is typical for lunge feeding (Goldbogen et al., 2007; Ware et al., 2011; Simon et al., 2012). In a typical lunge event, the whale moves slightly laterally through the prey layer/school or penetrates it with wide open mouth from below (Simon et al., 2012). Lunge feeding is conducted by Rorquals (family Balaenopteridae) (Pivorunas, 1979). Synchronous feeding behaviour has been observed by groups of 2–3 individuals of both humpback whales (Tyson et al., 2012) and fin whales (Nøttestad et al., in press). One can, therefore, speculate in whether these tracks may belong to such whales. Other tracks represent animals close to the surface (420 m depth) without any particular diving behaviour that may indicate what type of species they may represent, as all cetaceans need to spend time at the surface to breath. However, none of these tracks appear to represent more than a few animals in total over an area with radius of about 100 m. Therefore, these do not likely represent pilot whales or dolphins, as these usually occur in larger groups. Interpretation of our data is dependent on the size of the whale. The pulse length was in our case 1 ms, i.e. ∼1.5 m. Targets that are more than 0.5 pulse length (40.75 m) can, thus, theoretically be separated. In theory, larger whales produce echoes not only when the pulse hits the animal but also when the pulse hits the body wall on the opposite side before penetrating to the open sea. It is, thus, important to evaluate if observed multi-phase echoes are from two animals swimming in synchrony or double echoes from one whale. In the latter case, the data hold
information about the size (diameter) of the animal. Due to the features of lunge feeding behaviour we consider it highly probable that Obs. number 1 (Fig. 3) is a large whale with a diameter of 2– 4 m rather than two individuals swimming in close synchrony. Obs. numbers 17 and 59 (Figs. S6 and S8) are whales swimming in synchrony, but apparently the synchrony is reduced with distance (Figs. 6 and 7). Synchrony and imitation are important fields in behaviour studies on land, particularly for birds (Bates and Byrne, 2010). The difficulties of underwater observations prevented similar approaches for marine mammals, although camera techniques show promising development (Calambokidis et al., 2007). Active acoustics has a large potential that has not yet been fully utilised, and this paper shows that even opportunistic data recorded by an active acoustic system may support new information about synchrony and its function for feeding behaviour in whales. The analyses demonstrate that animals may swim close enough in the vertical plane to be interpreted as one target. Obs. number 59 (Fig. S8) indicates that horizontal separation might be much higher than vertical. As expected, synchrony is reduced with distance, but our data are too limited to really draw any conclusion on synchrony dynamics. We have indicated that about half of the dives are synchronous. This number should not be biased by our selection of dives as the material follows the choice of Doksæter et al. (2009). However, this result needs validation through a more systematic study where cetaceans are followed for a longer time period. We have seen that synchrony is initiated and interrupted at various depths and times during a dive, and thus, interpretation in a behaviour ecology context is difficult. Active acoustics has been used sporadically to study cetaceans including behaviour and acoustic properties (Bernasconi et al., 2011 and references therein). Acoustic target tracking with splitbeam technology is scarce and to our knowledge limited to a few
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papers (Doksæter et al., 2009; Bernasconi et al., 2011). The main reason is that acoustics normally is collected with hull mounted transducers and diving cetaceans under vessels in operation are scarce. Our data were collected opportunistically from a platform that was launched for studying fish behaviour. Thus, the material is limited and this paper should be looked upon as a methodological contribution to how active acoustics can be used to study behaviour of marine mammals in the future. The next step in our development includes an autonomous tracking system to enable automatic identification of marine mammal targets based on their acoustic target strength and behavioural characteristics. When the system has identified such a target the motorised transducer will automatically follow the target as long as it is located within the searching volume of the system (Fig. 8). Species identification could also be supported by passive acoustic identification (Oswald et al., 2003; Andre et al., 2011). Such a system will represent a new tool for studying whale behavioural characteristics in the presence of their prey field. Under such improved observation conditions retrieval of other details might also become realistic, for example tail beat frequency (Handegard et al., 2009), which was not possible to analyse with the present limited data. This methodological endeavour has demonstrated the potential of using active acoustic split-beam technology to extract whale behavioural characteristics including synchronous movements but also emphasised some of the difficulties in using the approach like double echoes from big animals and small sampling volume. Tailoring technology for the purpose will greatly enhance the chance for success. Acknowledgement The MAR-ECO project is thanked for financial support to collect these data. We are grateful to captains and crews on board RV G.O. Sars and RV James Clark Ross for their help in launching and retrieving the acoustic mooring. Peter Tyack at University of St. Andrews is thanked for comments and suggestions during the preparation of this paper. Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.dsr2.2013.06.013.
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Brede, R., Kristensen, F.H., Solli, H., Ona, O., 1990. Target tracking with a split-beam echo sounder. Rapp. P.-v. Réun. Cons. int. Explor. Mer 189, 254–263. Calambokidis, J., Schorr, G.S., Steiger, G.H., Francis, J., Bakhtiari, M., Marshal, G., Oleson, E.M., et al., 2007. Insights into the underwater diving, feeding, and calling behaviour of blue whales from a suction-cup-attached video-imaging tag (CRITTERCAM). Mar. Technol. Soc. J. 41, 19–29. Conradt, L., Roper, T.J., 2000. Activity synchrony and social cohesion: a fission– fusion model. Proc. R. Soc. B: Biol. Sci. 267, 2213–2218. Doksæter, L., Godø, O.R., Olsen, E., Nøttestad, L., Patel, R., 2009. Ecological studies of marine mammals using a seabed-mounted echosounder. ICES J. Mar. Sci. 66, 1029–1036. Engel, J., Lamprecht, J., 1997. Doing what everybody does? A procedure for investigating behavioural synchronization. J. Theor. Biol. 185, 255–262. Erbe, C., King, A.R., 2008. Automatic detection of marine mammals using information entropy. J. Acoust. Soc. Am. 124, 2833–2840. Foote, K.G., 1987. Fish target strengths for use in echo integrator surveys. J. Acoust. Soc. Am. 82, 981–987. Goldbogen, J.A., Pyenson, N.D., Shadwick, R.E., 2007. Big gulps require high drag for fin whale lunge feeding. Mar. Ecol. Prog. Ser. 349, 289–301. Handegard, N.O., 2007. Observing individual fish behaviour in fish aggregations: tracking in dense fish aggregations using a split-beam echosounder. J. Acoust. Soc. Am. 122, 177–187. Handegard, N.O., Patel, R., Hjellvik, V., 2005. Tracking individual fish from a moving-platform using a split-beam transducer. J. Acoust. Soc. Am. 118, 2210–2223. Handegard, N.O., Pedersen, G., Brix, O., 2009. Estimating tail-beat frequency using split-beam echosounders. ICES J. Mar. Sci. 66, 1252–1258. Kaartvedt, S., Rostad, A., Klevjer, T.A., Staby, A., 2009. Use of bottom-mounted echo sounders in exploring behaviour of mesopelagic fishes. Mar. Ecol. Prog. Ser. 395, 109–118. Knudsen, F.R., Gammelsæter, O.B., Kvadsheim, P.H., Nøttestad, L., 2008. Evaluation of fisheries sonar for whale detection in relation to seismic survey operations. Bioacoustics 17, 327–328. Metcalfe, J.D., Arnold, G.P., 1997. Tracking fish with electronic tags. Nature 387, 665–666. Nøttestad, L., Sivle, L.D., Krafft, B., Langård, L., Anthonypillai,V., Bernasconi, M., Langøy, H., Axelsen, B.E. Ecological aspects of fin- and humpback whale distribution during summer in the Norwegian Sea. Mar. Ecol., in press. Noren, S.R., Edwards, E.F., 2011. Infant position in mother–calf dolphin pairs: formation locomotion with hydrodynamic benefits. Mar. Ecol. Prog. Ser. 424, 229–236. Ona, E., 1999. Methodology for target strength measurements. ICES Coop. Res. Rep. 235, 1–59. Opdal, A.F., Godø, O.R., Bergstad, O.A., Fiksen, O., 2008. Distribution, identity, and possible processes sustaining meso- and bathypelagic scattering layers on the northern Mid-Atlantic Ridge. Deep Sea Res. II 55, 45–58. Oswald, J.N., Barlow, J., Norris, T.F., 2003. Acoustic identification of nine delphinid species in the eastern tropical Pacific Ocean. Mar. Mammal Sci. 19, 20–37. Pivorunas, A., 1979. Feeding mechanisms of baleen whales. Am. Sci. 67, 432–440. Senigaglia, V., Whitehead, H., 2012. Synchronous breathing by pilot whales. Mar. Mammal Sci. 28, 213–219. Senigaglia, V., de Stephanis, R., Verborgh, P., Lusseau, D., 2012. The role of synchronized swimming as affiliative and anti-predatory behaviour in longfinned pilot whales. Behav. Process. 91, 8–14. Simon, M., Johnson, M., Madsen, P.T., 2012. Keeping momentum with a mouthful of water: behaviour and kinematics of humpback whale lunge feeding. J. Exp. Biol. 215, 3786–3798. Tremblay, Y., Cherel, Y., 1999. Synchronous underwater foraging behaviour in penguins. Condor 101, 179–185. Tyack, P.L., 2008. Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. J. Comp. Psychol. 122, 319–331. Tyson, R.B., Friedlaender, A.S., Ware, C., Stimpert, A.K., Nowacek, D.P., 2012. Synchronous mother and calf foraging behaviour in humpback whales Megaptera novaeangliae: insights from multi-sensor suction cup tags. Mar. Ecol. Prog. Ser. 457, 209–220. Ware, C., Friedlaender, A.S., Nowacek, D.P., 2011. Shallow and deep lunge feeding of humpback whales in fjords of the West Antarctic Peninsula. Mar. Mammal Sci. 27, 587–605. Wenneck, T.L., Falkenhaug, T., Bergstad, O.A., 2008. Strategies, methods, and technologies adopted on the R.V. G.O. Sars MAR-ECO expedition to the MidAtlantic Ridge in 2004. Deep-Sea Res. II 55, 6–28.
Contents lists available at ScienceDirect
Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2
Synchronous behaviour of cetaceans observed with active acoustics Olav Rune Godø a,n, Lise Doksæter Sivle a, Ruben Patel b, Terje Torkelsen c a b c
Institute of Marine Research, P.P. Box 1870, 5817 Bergen, Norway CodeLab Bergen, Klostergaten 26, 5005 Bergen, Norway METAS, Nedre Åstveit 12, 5106 Bergen, Norway
art ic l e i nf o
a b s t r a c t
Available online 29 June 2013
Scientific split-beam echosounders are sensitive instruments for observing biomass densities and individual behaviour. Earlier studies have demonstrated that these instruments can be used to study diving behaviour of cetaceans. In this paper, we go into more detail about the recorded signal to see if and how acoustic split-beam data can be used to extract information about synchronous behaviour and other species related characteristics. Data of several cetacean individuals were collected by a moored echosounder pinging upwards from about 900 m in the Charlie Gibbs Fracture Zone. In this paper, we discuss methodological issues associated with using split-beam tracking of large marine animals. Further we demonstrate that target tracking of cetaceans can be used to study solo dives as well as behavioural synchrony. We also show that paired signals can easily be interpreted as false synchrony due to the size of the animals. In such cases a rough estimate of the diameter, and hence size, of the animals can be estimated. We emphasise on four examples that clarify methodological challenges including synchronous swimmers as well as large single cetaceans that might be interpreted as two synchronous swimmers. The applied technology requires that the animals remain in a narrow acoustic beam for long enough time to extract behavioural information. The technology can be improved by developing automatic tracking of cetaceans with a steerable transducer. This will substantially increase the search volume and enable tracking of cetaceans over longer periods and thus, produce more realistic information about the whale behaviour. & 2013 Elsevier Ltd. All rights reserved.
Keywords: Whale behaviour Synchrony Active acoustics Tracking Feeding
1. Introduction Synchronous movements are common features in terrestrial and marine social animals (Engel and Lamprecht, 1997; Conradt and Roper, 2000). Whereas such behavioural characteristics often are associated to anti-predator tactics it might also be an efficient hunting and teaching strategy (Senigaglia and Whitehead, 2012; Senigaglia et al., 2012; Tremblay and Cherel, 1999). Synchrony feeding may ease energetic cost due to hydrodynamic advantages and has particularly been observed in mother–calf pairs (Noren and Edwards, 2011; Tyson et al., 2012). Qualitative and quantitative studies of synchronous behaviour on land can be done with simple visual methods, but similar results from underwater realm have been inferred from indirect method like tagging (Tremblay and Cherel, 1999; Tyson et al., 2012) or from visual observation at surface (Senigaglia and Whitehead, 2012).
n
Corresponding author. E-mail addresses: [email protected] (O.R. Godø), [email protected] (L.D. Sivle), [email protected] (R. Patel), [email protected] (T. Torkelsen). 0967-0645/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2013.06.013
Direct observation of detailed behavioural patterns of individual marine fishes has been enabled by tagging (Metcalfe and Arnold, 1997) and by split-beam acoustic target tracking techniques (Handegard, 2007; Kaartvedt et al., 2009). Active acoustics has also been used to observe marine mammals (Doksæter et al., 2009) as well as birds (Benoit-Bird et al., 2011). Acoustic split-beam echosounder techniques (Brede et al., 1990; Ona, 1999; Foote, 1987) allow three dimensional positioning of individuals in the beam volume. Distances to target from the four sectors of the split-beam transducer are estimated from the differences in the phase angle (time delay) of the backscattered signal as observed at these four sectors (see Supplementary video). These distances are used to triangulate the target position in the beam. Behavioural characteristics of fish movement in time and space have been developed using target tracking techniques (Handegard et al., 2005). The pulse (1 ms about 1.5 m) travels through the acoustic beam and when several individuals are present in the same pulse volume the phase angle will show high variability across samples and hence undefined position. When observing samples with integrity (co-variation) in the phase information of the backscattering signal it can be defined as a valid target. The target tracking algorithm then allocates accepted
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targets to specific individuals, thus, allowing their trajectories to be drawn. High ping to ping variation is often caused by multiple individuals simultaneously present in the same pulse volume. Integrity, i.e. smooth ping to ping changes of the phase angles, is interpreted as consistency in target movement, as expected for the swimming trajectory of a fish. Supplementary material related to this article can be found online at http://dx.doi.org/10.1016/j.dsr2.2013.06.013. This paper focuses on the methodology employed in four studies on diving animals with different behavioural characteristics. Our aim is to demonstrate that active acoustic split-beam technology can be used to study detailed individual and synchronous behaviour of top predators in the marine environment and to report unique behavioural recordings of whales apparently foraging over the mid-Atlantic ridge. The method allows the observation of animals and records fine scale behavioural characteristics such as feeding to the full depth of diving capabilities without prior selection and tagging process.
2. Materials and methods In this paper, the targets are tracked manually and the tracks are used to study whale behaviour. Systematic changes in acoustic backscattering strength of tracked fish enable the characterisation of fine details like tail beat frequency of single fish (Handegard et al., 2009). We use tracked targets to study further the data presented by Doksæter et al. (2009) to extract details about behaviour of diving cetaceans with particular emphasis on dives of multiple individuals. Dives were studied in detail to extract quantitative information on synchronous movement patterns. Data were collected with a moored split-beam echosounder launched on July 22, 2004, at N51131.6′ and W030119.9′ at a bottom depth of 920 m. The water column from 910 m to surface (Fig. 1) was observed during a period of 10 months until end of May 2005 (Wenneck et al., 2008). The observation frequency and angle were 38 kHz and 71, respectively, and the ping rate was 30 min 1. Thus, the footprint diameter of the acoustic beam at surface was 110 m and gradually reduced to about 100 m at 100 m depth, which includes the depth range of all dives in our data set (Table 1). Since the animals swam in and out of the beam at various depths, the observation time of the individual targets varied a lot. Only acoustic targets (cetaceans) satisfying certain criteria were included in the analysis (see Table 2), but their identity cannot be established from this analysis. The target tracking principle supported by the split-beam transducers utilises the ability of the transducer to record the echoes separately at four quadrants of the transducer. The
principle geometry is illustrated in Fig. 2 and accordingly, the arrival angle (θ) can be calculated θ ¼ sin 1 ðΔr=dÞ The difference in range between arrivals at the two transducer quadrants can be calculated using the arrival time delay or based on the phase shift of the signal at arrival. This is a far field approximation which is valid for all targets analysed in this paper. The selected acoustic targets, likely to represent one or more cetaceans, in our analysis (see Table 1) are classified under Category 1 (the best) by Doksæter et al. (2009). The analysis includes three consecutive processes:
Visual interpretation: Splitting observations into lone-divers (single
individuals) and multiple-divers (more than one animal). In some instances, both types of echoes were included in the same dive and in such cases they were separated and identified as single- and multi-phases, where single-phase includes one animal and multiphase includes two or more (see Figs. 3 and S1–S12). Quantitative interpretation: We studied the echoes from lonedivers and single-phase divers further to distinguish between single targets when they satisfy criteria as described by Handegard et al. (2009) and multiple targets if not satisfying these criteria (see the previous paragraph). Tracks were isolated manually in the echogram (see Fig. 3). Then a target detector was applied to each of the isolated regions to extract valid targets using the settings given in Table 2. In some instances two detections were observed in one ping inside one region. The position data from these detections were averaged. Quantitative assessment of synchronous behaviour: Finally, based on the available accepted single target measurements, we evaluated synchrony in whale behaviour for multiple-divers and multi-phase divers based on the similarity in behaviour of neighbouring animals. In our case, the observed phase angles are converted to distances from the centre of the beam, and correlation between the estimated distances over time is used to evaluate synchrony. These distances also allow the study of impact of proximity on synchrony.
3. Results Cetaceans were repeatedly observed diving from the surface to acoustic layers at 50–100 m comprising mesopelagic fish such as Muller’s pearlside (Maurolicus mulleri) (Opdal et al., 2008), during the time series. Along with dives to well-defined acoustic layers of
Fig. 1. A sketch of the acoustic buoy located at 910 m depth pointing upward (left panel). Right panel shows a zoomed echogram from surface to 200 m. There are three whale dives (A, B, and C) at the echogram appearing as clear green/cyan (grey) vertical moving lines. The maximum diving depth is 75 m.
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Table 1 Overview of the analysed targets (see also Figs. S1–S12). Duration refers to the longest track when multiple targets are present in the figures. Lone and synchronous refer to the number of dives defined as lone dives and synchronous dives. NA, not applicable. Date
Obs. number
Time (UTC)
Duration (min)
Max diving depth (m)
Number of animals
Figure
Lone
Synchronous
10.08.2004 05.09.2004 05.09.2004 21.09.2004 03.11.2004 03.11.2004 26.11.2004 27.11.2004 27.11.2004 16.12.2004 18.02.2005 10.03.2005 Sum
Obs. 1 Obs. 5 Obs. 70 Obs. 11 Obs. 17 Obs. 45 Obs. 59 Obs. 2 Obs. 3 Obs. 62 Obs. 9 Obs. 68
16:05 18:19 19:29 17:54 00:23 03:02 13:14 00:21 04:51 04:02 11:28 08:36
2 2 2 3 4 2 1 2 2 6 3 2
72 14 44/85 19 71 14 26 30 55 60 16 18
3a 2 3 3 6 2 2 2 3 3 3 2
S1 S1 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12
2 1 3 3 NA NA NA NA NA 1 1 NA 11
1 NA 1 NA 3 1 1 1 1 1 1 1 12
a
It is four animals if track C is accepted as a multi-phase (see text).
Table 2 Settings for the single target detection in Large Scale Survey System software. TS is acoustic target strength. Variable (LSSS)
Setting
Explanation
MinTS MaxTS PulsLengthDeterminationLevel MinEchoLength MaxEchoLength MaxGainCompensation
30 10 5 0 3.8 10
Minimum TS value to be detected (dB) Maximum TS value to be detected (dB) Pulse length determination level (dB) Minimum echo length relative to pulse length Maximum echo length relative to pulse length Maximum gain compensation (dB)
Fig. 2. Illustration of the geometry of the received echo and how this can be used to estimate position of the target. The arrival angel of an acoustic signal arriving at two transducer quadrants is represented by two lines. θ represents the arrival angle which can be estimated based on the range difference (Δr) and distance between the transducer quadrants (d).
potential food, some shallow dives of individuals and groups that were probably travelling over the location (Figs. S1–S12) were also recorded. In this paper, we gave particular attention to few of the deeper dives, however, some key data and visual interpretation are associated with echograms of additional tracks (see Table 1 and Figs. S1–S12). A visual survey of the area was conducted in July 2004, and the species observed in the area around Charlie Gibbs Fracture Zone is shown in Table 3. 3.1. Visual interpretation Some details about the tracks given particular attention in this paper are summarised in Table 1 (Obs. numbers 1, 3, 17, and 59).
The tracks we interpreted and classified in accordance with the three categories are described in Section 2 (lone-divers, singleand multi-phases) (see also Figs. 3 and 4). The analysis under Section 3.2 follows this classification. The three dives in Fig. 3 are the same as indicated in Fig. 1 but observed with a different resolution. While A and B apparently are lone-divers, C looks like a lone diver during the start but the later split indicates that this is a multi-phase dive changing to two single-phase dives. Based on a ping to ping study of the tracks, we separated the tracks or part of tracks by red boxes as indicated in Fig. 3, lower panel. Similar categorisation is illustrated for Obs. numbers 17 (Fig. S6 track C) and 59 (Fig. S8) and extracted splitbeam data were used for the further analysis. Fig. 4, upper panel, shows a lone diver splitting into two and later three separate tracks. Panels A and B present variation in the phase angles and demonstrate that these angles stand out from the normal variability and thus, indicate that these tracks represent individuals swimming close together. 3.2. Quantitative interpretation The visual interpretations in Section 3.1 illustrate that the echogram does not necessarily reflect the truth about the number of animals; both two and three animals emerged from what appeared to be a single individual. It should be kept in mind that the echogram separates animals only in the vertical direction. Vertically resolved individuals could be separated by large horizontal distances as the footprint of the acoustic beam is on the order of 100 m in diameter at the observation depth. Thus, animals that appear visually close are not necessarily synchronous swimmers. Furthermore, the visually interpreted lone-divers could theoretically be composed of more than one animal well separated horizontally in the beam but included in the same pulse volume when at similar depth. The target tracking approach may solve these issues. Such tracking must be done with settings adjusted to the observation situation, and the settings in Table 2 have been
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Fig. 3. Upper panel: echogram of Obs. number 1. This observation consists of three separate tracks: A, B and C. A and B are typical lone-divers, while C appears like a lone diver during the start when swimming through a layer of prey. The lone diver apparently split into synchronously swimming single-phase divers during ascent to the surface. Thus, the first part of the track is a multi-phase dive, while the second part is two single-phases. Lower panel: details of track C. T1 is the multi-phase when two cetaceans are swimming together in a prey layer. T2 and T3 are the single-phases, when the two animals separate and ascent towards the surface in a synchronous manner. Red (grey) boxes show the separated track, and black marks indicate identified accepted single target tracks as defined in LSSS (Table 2).
Table 3 Visual observations of marine mammals from the RV G.O. Sars at the Charlie Gibbs Fracture Zone in the area of the moored echosounder on Leg 1 of the Mar-Eco cruise (Wenneck et al., 2008) 17–18 June 2004. Common name
Scientific name
Minke whale
Balaenoptera acutorostrata Baleanoptera borealis Balaenoptera physalus Globicephala melas Lagenorhynchus acutus Mesoplodon sp. Physeter macrocephalus Balaenopetera sp.
Sei whale Fin whale Pilot whale White-sided dolphins Beaked whale Sperm whale Unidentified baleen whale
Total number
Number of observations
1
1
44 3
31 3
46 30
3 2
3 12
3 8
5
5
demonstrated to perform well in the current situation. For example tracking of large animals (45 m) such as cetaceans requires a higher setting of echo length and acoustic target strength due to their size. The proportion of the signals accepted as single targets is important for the evaluation and so is the stability of recorded single target information that is used to assess the absolute position of cetaceans in relation to each other. As seen in Fig. 3, a high portion of the pings are accepted by the tracker as single target, but not all. Concerning stability of the target information, we see that the phase angles (both directions) of the tracks, appearing from the grey scale in Fig. 4, stand out from the phase angles of the rest of the pixels in the echogram with respect to the stability and consistency. This indicates coordinated movements of individuals that are close to each other. Similar information is available for all dives.
3.3. Quantitative assessment The information extracted in Section 3.2 was used to assess the exact position of the targets with respect to the depth and position in the beam (phase angles of the signal). Obs. number 1 (Fig. 3) was split into single-phase and multi-phase tracks and the position in the beam estimated (Fig. 5). The very smooth parallel movements of the single-phase observations indicate parallel swimming animals with a distance of about 2–3 m. The quality of the positioning of the track is also confirmed by high correlation between x and y distances (converted from phase angles) (Table 4). Similar calculations are available for the Obs. numbers 17 and 58. The tracks of Obs. number 17 are more than 10 m apart vertically (Fig. 6) and the x and y distances are highly correlated (simple linear regression, Table 4), although r2 is lower than for Obs. number 1. The animals of Obs. number 58 are relatively close together vertically (2–4 m) but are separated horizontally by as much as 20–40 m (Fig. 7). Distances from the beam centre are loosely correlated in the x-direction but strongly correlated in the y-direction. In Table 1, we have given our interpretation of number of animals included in the studied examples (Figs. S1–S12) and number of dives defined as lone and synchronous dives. Based on our material it is indicated that about half of the dives are synchronous.
4. Discussion Our results demonstrate that a target tracking technique can be used to study diving behaviour of cetaceans and synchronous movements. The interaction between visual interpretation of the echograms and statistical analysis of the target information enabled the quantification of behaviour and interaction. We can see how individuals behave in relation to each other and this might have a range of applications with respect to the
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Fig. 4. Upper panel: echogram of Obs. number 3 showing three animals diving in synchrony. During the first part of decent the animals are inseparable. Then apparently three single-phase dives emerge. One of the animals separates from the two others, which continue to move close together from a depth of ∼20 m, thus, becoming a multiphase. Lower panel shows the phase angles where the diving whale stands out with consistent changes.
Table 4 Consistency in the variation of distance from centre (equivalent to phase angle) of Obs. numbers 1, 17 and 59 given as the correlation coefficient (r2) of the linear regression between comparable angles.
Fig. 5. Obs. number 1 with multi- (circles) and single-phase tracks (pyramid and cubes) showing the movements in the beam from 70 m to surface. Axis values are in metres. Range refers to surface as zero while x and y refer to centre of beam as zero.
understanding of individual and group behaviours in relation feeding, social behaviour, learning, etc. In our study, we used an active echosounder system operating at 38 kHz. This is within the hearing range of many cetaceans and thus, we cannot exclude the possibility that the acoustic system influenced the target behaviour. For example, our system received several instances of pulses of sound (noise) that could be whale vocalisations imitating the echosounder (see Fig. S5). Whale imitation of sounds, also anthropogenic, is a part of their learning and habituation process (Tyack, 2008), and low
Obs. number
X (m)
Y (m)
Number of parallel observations
1 17 59
0.96 0.82 0.10
0.90 0.79 0.96
18 9 9
power echosounder pulses have over time likely become part of the normal soundscape of marine animals, including cetaceans. It has e.g. been demonstrated that scientific sonars and echosounders do not affect the behaviour of killer whales (Knudsen et al., 2008), and the behavioural impact of the echosounder is, thus, considered low or negligible. The use of acoustic target tracking as a means of species or group identification requires some kind of validation. This could be a visual observation at surface or passive acoustic recording systems that identify animals through their vocalisation (see e.g. Erbe and King, 2008; Andre et al., 2011). During a survey along the mid-Atlantic ridge in summer of 2004 (www.mar-eco.no), several species of cetaceans were found to occupy the Charlie Gibbs Fracture Zone (Table 3). The lack of any kind of positive confirmations, such as simultaneous visual observations together with the novelty of the method, makes any attempts to verify the cetacean species of the recordings presented in this study highly speculative. However, based on the list of occurring species in Table 3, together with dive depth, shape of the track and the observed number of animals, we may do some speculations. Diving depth of the tracks varies from 14 to 85 m and is within the diving range of all the species represented in Table 3. Some of the tracks show diving towards and into distinct prey layers e.g.
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Fig. 6. Time (observation number)–depth plot of the track information of Obs. number 17. Double arrow line indicates a range of 10 m.
Fig. 8. Autonomous target follower based on a moving transducer (T) directing a searching beam (B) either systematically through a searching pyramid (opening angle of 601) or actively following a specific target over time. The searching volume increases with range (h) and at 500 m range sides in the searched rectangle (a and b) will be more than 800 m.
Fig. 7. Distances from centre of beam of the single-phase tracks of Obs. number 59. Double arrow line indicates a range of 30 m.
tracks A and C in Fig. 1, which have a dive with a U signature, with the dive ending just underneath a prey layer, which is typical for lunge feeding (Goldbogen et al., 2007; Ware et al., 2011; Simon et al., 2012). In a typical lunge event, the whale moves slightly laterally through the prey layer/school or penetrates it with wide open mouth from below (Simon et al., 2012). Lunge feeding is conducted by Rorquals (family Balaenopteridae) (Pivorunas, 1979). Synchronous feeding behaviour has been observed by groups of 2–3 individuals of both humpback whales (Tyson et al., 2012) and fin whales (Nøttestad et al., in press). One can, therefore, speculate in whether these tracks may belong to such whales. Other tracks represent animals close to the surface (420 m depth) without any particular diving behaviour that may indicate what type of species they may represent, as all cetaceans need to spend time at the surface to breath. However, none of these tracks appear to represent more than a few animals in total over an area with radius of about 100 m. Therefore, these do not likely represent pilot whales or dolphins, as these usually occur in larger groups. Interpretation of our data is dependent on the size of the whale. The pulse length was in our case 1 ms, i.e. ∼1.5 m. Targets that are more than 0.5 pulse length (40.75 m) can, thus, theoretically be separated. In theory, larger whales produce echoes not only when the pulse hits the animal but also when the pulse hits the body wall on the opposite side before penetrating to the open sea. It is, thus, important to evaluate if observed multi-phase echoes are from two animals swimming in synchrony or double echoes from one whale. In the latter case, the data hold
information about the size (diameter) of the animal. Due to the features of lunge feeding behaviour we consider it highly probable that Obs. number 1 (Fig. 3) is a large whale with a diameter of 2– 4 m rather than two individuals swimming in close synchrony. Obs. numbers 17 and 59 (Figs. S6 and S8) are whales swimming in synchrony, but apparently the synchrony is reduced with distance (Figs. 6 and 7). Synchrony and imitation are important fields in behaviour studies on land, particularly for birds (Bates and Byrne, 2010). The difficulties of underwater observations prevented similar approaches for marine mammals, although camera techniques show promising development (Calambokidis et al., 2007). Active acoustics has a large potential that has not yet been fully utilised, and this paper shows that even opportunistic data recorded by an active acoustic system may support new information about synchrony and its function for feeding behaviour in whales. The analyses demonstrate that animals may swim close enough in the vertical plane to be interpreted as one target. Obs. number 59 (Fig. S8) indicates that horizontal separation might be much higher than vertical. As expected, synchrony is reduced with distance, but our data are too limited to really draw any conclusion on synchrony dynamics. We have indicated that about half of the dives are synchronous. This number should not be biased by our selection of dives as the material follows the choice of Doksæter et al. (2009). However, this result needs validation through a more systematic study where cetaceans are followed for a longer time period. We have seen that synchrony is initiated and interrupted at various depths and times during a dive, and thus, interpretation in a behaviour ecology context is difficult. Active acoustics has been used sporadically to study cetaceans including behaviour and acoustic properties (Bernasconi et al., 2011 and references therein). Acoustic target tracking with splitbeam technology is scarce and to our knowledge limited to a few
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papers (Doksæter et al., 2009; Bernasconi et al., 2011). The main reason is that acoustics normally is collected with hull mounted transducers and diving cetaceans under vessels in operation are scarce. Our data were collected opportunistically from a platform that was launched for studying fish behaviour. Thus, the material is limited and this paper should be looked upon as a methodological contribution to how active acoustics can be used to study behaviour of marine mammals in the future. The next step in our development includes an autonomous tracking system to enable automatic identification of marine mammal targets based on their acoustic target strength and behavioural characteristics. When the system has identified such a target the motorised transducer will automatically follow the target as long as it is located within the searching volume of the system (Fig. 8). Species identification could also be supported by passive acoustic identification (Oswald et al., 2003; Andre et al., 2011). Such a system will represent a new tool for studying whale behavioural characteristics in the presence of their prey field. Under such improved observation conditions retrieval of other details might also become realistic, for example tail beat frequency (Handegard et al., 2009), which was not possible to analyse with the present limited data. This methodological endeavour has demonstrated the potential of using active acoustic split-beam technology to extract whale behavioural characteristics including synchronous movements but also emphasised some of the difficulties in using the approach like double echoes from big animals and small sampling volume. Tailoring technology for the purpose will greatly enhance the chance for success. Acknowledgement The MAR-ECO project is thanked for financial support to collect these data. We are grateful to captains and crews on board RV G.O. Sars and RV James Clark Ross for their help in launching and retrieving the acoustic mooring. Peter Tyack at University of St. Andrews is thanked for comments and suggestions during the preparation of this paper. Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.dsr2.2013.06.013.
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