Author response: Range-dependent flexibility in the acoustic field of view of echolocating porpoises (Phocoena phocoena)
2015-03-19

Article Figures and data Abstract eLife digest Introduction Results Discussion Materials and methods Data availability References Decision letter Author response Article and author information Metrics Abstract Toothed whales use sonar to detect, locate, and track prey. They adjust emitted sound intensity, auditory sensitivity and click rate to target range, and terminate prey pursuits with high-repetition-rate, low-intensity buzzes. However, their narrow acoustic field of view (FOV) is considered stable throughout target approach, which could facilitate prey escape at close-range. Here, we show that, like some bats, harbour porpoises can broaden their biosonar beam during the terminal phase of attack but, unlike bats, maintain the ability to change beamwidth within this phase. Based on video, MRI, and acoustic-tag recordings, we propose this flexibility is modulated by the melon and implemented to accommodate dynamic spatial relationships with prey and acoustic complexity of surroundings. Despite independent evolution and different means of sound generation and transmission, whales and bats adaptively change their FOV, suggesting that beamwidth flexibility has been an important driver in the evolution of echolocation for prey tracking. https://doi.org/10.7554/eLife.05651.001 eLife digest Bats and toothed whales such as porpoises have independently evolved the same solution for hunting prey when it is hard to see. Bats hunt in the dark with little light to allow them to see the insects they chase. Porpoises hunt in murky water where different ocean environments can quickly obscure fish from view. So, both bats and porpoises evolved to emit a beam of sound and then track their prey based on the echoes of that sound bouncing off the prey and other objects. This process is called echolocation. A narrow beam of sound can help a porpoise or bat track distant prey. But as either animal closes in on its prey such a narrow sound beam can be a disadvantage because prey can easily escape to one side. Scientists recently found that bats can widen their sound beam as they close in on prey by changing the frequency—or pitch—of the signal they emit or by adjusting how they open their mouth. Porpoises, by contrast, create their echolocation clicks by forcing air through a structure in their blowhole called the phonic lips. The sound is transmitted through a fatty structure on the front of their head known as the melon, which gives these animals their characteristic round-headed look, before being transmitted into the sea. Porpoises would also likely benefit from widening their echolocation beam as they approach prey, but it was not clear if and how they could do this. Wisniewska et al. used 48 tightly spaced underwater microphones to record the clicks emitted by three captive porpoises as they approached a target or a fish. This revealed that in the last stage of their approach, the porpoises could triple the area their sound beam covered, giving them a 'wide angle view' as they closed in. This widening of the sound beam occurred during a very rapid series of echolocation signals called a buzz, which porpoises and bats perform at the end of a pursuit. Unlike bats, porpoises are able to continue to change the width of their sound beam throughout the buzz. Wisniewska et al. also present a video that shows that the shape of the porpoise's melon changes rapidly during a buzz, which may explain the widening beam. Furthermore, images obtained using a technique called magnetic resonance imaging (MRI) revealed that a porpoise has a network of facial muscles that are capable of producing these beam-widening melon distortions. As both bats and porpoises have evolved the capability to adjust the width of their sound beam, this ability is likely to be crucial for hunting effectively using echolocation. https://doi.org/10.7554/eLife.05651.002 Introduction Echolocation has evolved independently multiple times in mammals and birds (Kellogg et al., 1953; Griffin, 1958; Konishi and Knudsen, 1979; Griffin and Thompson, 1982), and allows these animals to orient under conditions of poor lighting. However, only toothed whales (henceforth 'whales') and laryngeally echolocating bats (henceforth 'bats') use echolocation to detect, locate, and track prey. In these groups, echolocation signals are primarily ultrasonic (>20 kHz) and are among the most intense biological sounds in water and in air (Madsen and Surlykke, 2013). These characteristics mean that in uncluttered spaces these predators can detect small prey many body-lengths ahead of them. Key to increasing the effective sensory range of biosonar is a directional sound beam (i.e., a narrow volume of forwardly ensonified space), which increases intensity along the acoustic axis and reduces ensonification of objects off-axis. It has recently been proposed that the advantages of a narrow sonar beam while in search of prey may have been the primary driver for the evolution of high frequency sonar signals in both whales and bats (Koblitz et al., 2012; Jakobsen et al., 2013; Madsen and Surlykke, 2013). As whales and bats close in on prey, both are thought to concurrently decrease signal intensity and auditory sensitivity to partially compensate for reduced transmission loss (Hartley, 1992; Au and Benoit-Bird, 2003; Supin et al., 2004; Linnenschmidt et al., 2012; Madsen and Surlykke, 2013), while increasing the signal emission rate for faster updates on prey location (Griffin, 1958; Morozov et al., 1972; Au, 1993). Both groups terminate prey pursuits with a low intensity, high repetition rate sequence of echolocation signals called a buzz (see ref. [Madsen and Surlykke, 2013] for review). Signal production rates characteristic of buzzes have likely evolved in these echolocators to facilitate close range prey tracking. However, for a given sonar beam, effective beam diameter will decrease as the distance between predator and prey diminishes. Thus, while a directional sound beam enables longer detection range by restricting the acoustic field of view (FOV), it may be disadvantageous to the echolocator at short ranges, as moving prey may easily vanish at the periphery of the FOV. Directionality increases with aperture size (e.g., a bat's gape) and signal frequency (Au, 1993) and both factors appear to be exploited by some bats to modify their beam (Surlykke et al., 2009; Jakobsen and Surlykke, 2010). Unlike bats, whales do not generate echolocation signals in the larynx nor do they emit them through the mouth or the nares (Ridgway et al., 1980; Cranford et al., 1996). Instead, whales have evolved specialized sound-producing structures, the phonic lips, located high in the blowhole (Figure 1). An echolocation click is generated by pneumatic actuation of the phonic lips as pressurized air is forced past them (Cranford et al., 1996). The resulting sound pulse propagates into the fatty melon and is transmitted into the water as a directional beam (Au et al., 1986). While the exact function of the melon is not known, its size and properties are expected to affect the radiation pattern of sound from the head (Varanasi et al., 1975; Aroyan et al., 1992; Harper et al., 2008). As the bulbous melon fills a large proportion of the forehead (Figure 1), the diameter of the head has come to be considered indicative of radiating aperture size (Au et al., 1999). Figure 1 Download asset Open asset Transverse MRI scans of a young harbour porpoise. The scale bars indicate 5 cm (bar in B applies also to C and D). The caudal part of the melon (yellow, A) abuts against layers of connective tissue, muscles, and tendons (red, A) forming a dense theca, which, along with the skull and a collection of nasal air sacs, reflect the vibrations that originate in the phonic lips (light brown, A) into the melon (Aroyan et al., 1992; Cranford et al., 1996). The melon is under control of highly developed facial musculature (Harper et al., 2008; Huggenberger et al., 2009). The fibers and tendons of the muscles (Mu) associated with the melon (Me) lie at oblique angles relative to the frontal, transverse, and sagittal body planes (Harper et al., 2008; Huggenberger et al., 2009). The actions of these richly innervated muscles can change the three-dimensional shape and/or stiffness of the melon (Harper et al., 2008; Huggenberger et al., 2009), and thus likely adjust the properties of the emitted sound. https://doi.org/10.7554/eLife.05651.003 Compared to bats, whales exhibit little flexibility in the frequency content of their echolocation signals (Madsen and Surlykke, 2013). We might therefore assume whales are capable of only small changes in beam directionality (Au et al., 1995) and thus be limited to a rather fixed FOV (Au et al., 1999). Yet, given that whales echolocate prey over much longer ranges than bats (Madsen and Surlykke, 2013) and are capable of making much narrower beams (Au et al., 1999; Surlykke et al., 2009; Koblitz et al., 2012; Jakobsen et al., 2013), such a constraint is hard to reconcile with the disadvantages associated with a fixed beamwidth during close tracking of prey. In bats, pursuit is often over quickly, often with less than 500 ms elapsing between prey detection and interception (Kalko, 1995). Prey pursuits by whales can last many seconds (Johnson et al., 2004) (Figure 2). Accordingly, we hypothesize that long buzzes in which the whale might follow its target from an uncluttered water column to a highly cluttered sea floor (Figure 2), and back again, may demand greater beam plasticity than is found in bats. Figure 2 Download asset Open asset Long terminal phase of prey pursuit by an echolocating harbour porpoise. (A) Echogram (see 'Material and methods': Live prey capture) displaying sonar clicks and echoes recorded by an acoustic tag attached to the animal just behind its blowhole (Johnson et al., 2004). y-axis (left) indicates time elapsed from emitted clicks to returning echoes, expressed also as target range (right). Clicks emitted at rates corresponding to inter-click intervals shorter than 3.3 ms time-window are displayed repeatedly. The color scale indicates signal energy from blue (faint) to red (intense). As pursuit proceeds from water column (0.7–1.1 m from surface, 2–2.5 m above sea floor) to sea bottom the immediate acoustic scene becomes more cluttered with complex bottom echoes shortly following fish echoes (from −9 s onwards). (B) Inter-click intervals color-coded for relative apparent output level (RAOL; [Wisniewska et al., 2012]) of signals as recorded by the tag. RAOL variation may stem from rapid head movements, source level adjustments, and/or beam directionality changes (with less energy reaching the tag from a narrow beam). On two occasions, when the fish escaped into the open space of the water column (at −16 s and −13 s), the porpoise increased its ICIs significantly, beyond the values considered as buzz (Wisniewska et al., 2012). However, when the fish escaped to similar distances while being at the bottom (and thus moving in arguably a more predictable way) the porpoise increased the ICIs only slightly, which might point to anticipatory acoustic tracking on the part of the echolocating animal. https://doi.org/10.7554/eLife.05651.004 Corroborating this hypothesis, most of the reported estimates of toothed whale beam patterns show relatively large variability (Evans, 1973; Au et al., 1986, 1987, 1995; Koblitz et al., 2012). Furthermore, a bottlenose dolphin was recently observed to steer, and modify the width of, its sonar beam when stationed on a bite plate and presented with targets displaced by large angles with respect to its body axis (Moore et al., 2008). The dolphin was proposed to use two mechanisms as means of beamwidth modulation: (i) phase shifting between two pairs of phonic lips dually actuated for generation of a single click and/or (ii) manipulation of the volume and geometry of the melon and the associated air-sacs. However, the latest experimental data suggest that dolphins use a single pair of phonic lips to produce echolocation signals (Au et al., 2012; Madsen et al., 2013; Finneran et al., 2014) and that the strong amplitude dependence of dolphin click spectra gives rise to a variable beam pattern, with more directional signals at higher source levels (Finneran et al., 2014). Hence, it remains unclear how and under what circumstances a bottlenose dolphin modulates the width of its sound beam, and whether other whale species, with more stereotyped sonar signals, such as porpoises, are capable of similar beamwidth changes. In this study, we set out to test the hypothesis that whales can change their FOV adaptively during prey interception. To that end, we used two complementary experiments to record the beam pattern and signal frequency content of echolocation clicks from harbour porpoises (Phocoena phocoena) closing in on targets. Additionally, we obtained magnetic resonance imaging on a dead harbour porpoise to visualize the sound generating structures, the fatty melon and the associated musculature and present video demonstrating melon deformations in an actively echolocating harbour porpoise. Results In experiment 1, three captive porpoises were recorded individually using a linear horizontal array of 8 hydrophones spaced 60 cm apart and submerged 75 cm below the water's surface, as the porpoises captured dead fish (Video 1). This setup (Figure 3A) allowed us to quantify the animals' beam patterns over long ranges as they approached and intercepted natural targets free-floating in the water column. A total of 16 trials were recorded for the three animals (5–6 trials/porpoise). Only trials in which the porpoises swam directly towards the centre of the array were analyzed, amounting to two trials for Freja and Eigil and one trial for Sif (a total of 75 clicks). Data from the two porpoises, Freja and Eigil, recorded during buzzes show that they could up to triple the width of their sonar beam as they approached prey (median difference of 7.85° for four trials: from a mean of 12.9° (6.6°–30.5°, with the large beamwidths produced at short target ranges, Figure 3B) during regular clicking (ICI >13 ms; [Wisniewska et al., 2012]) to 19.3° (10.2°–28.9°) during buzzes (ICI ≤13 ms; [Wisniewska et al., 2012]), Figure 3B). However, limitations in the linear array recordings prevented us from drawing strong conclusions about the exact extent of beam widening: the angular resolution was 4–12° and there was no way to precisely determine the vertical direction of the porpoise beam. Even though the video observations indicated that the vertical direction of the porpoise head was not changing with range to the array, this could not be adequately quantified. Video 1 Download asset This video cannot be played in place because your browser does support HTML5 video. You may still download the video for offline viewing. Download as MPEG-4 Download as WebM Download as Ogg A representative trial from experiment one. Video shows a porpoise capturing fish in front of the linear hydrophone array. Hydrophones were lowered to a depth of 75 cm along the short side of the pool. Prior to the experiment the blindfolded (i.e., wearing opaque silicone eyecups) porpoise was stationed at the opposite end of the pool. As freshly thawed fish were introduced approx. 3 m from the array, the animal was cued to perform the capture task. The porpoise did not roll throughout the approach. Thus, the observed beam changes could not result from the beam not being rotationally symmetric and the animal rolling consistently during the buzz. https://doi.org/10.7554/eLife.05651.005 Figure 3 Download asset Open asset Porpoise biosonar beam widens at short target ranges. 3 dB beamwidth recorded in two experimental setups: (A, B) three harbour porpoises closing on prey and (C, D) a harbour porpoise approaching an aluminum sphere target. (A, C) show reconstructed porpoise locations for clicks fulfilling inclusion criteria in one trial per array configuration. Targets and their projections in the x–y plane are marked with dark-blue filled and open circles, respectively. For the small array recordings (light blue in C), the target was displaced outward to 0.4 m from the array to maintain high spatial resolution at short ranges. (B) Data collected using a horizontal array with effective angular resolution (EAR) of ∼12° at ranges of target interception (N = 75). Data points from Freja, the porpoise participating in experiment two, are represented with circles. (D) Data gathered with star-shaped arrays in two configurations: large (red in C), for long-range recordings (>1.3 m from array to sound source, squares, N = 34) and small (light blue in C), for greater resolution at short ranges (<2 m from array to sound source, circles, N = 458) (see Figure 4—figure supplement 1 for a detailed view of hydrophone spacing in the two array configurations). Hydrophone spacing provided EAR of ∼5° at the shortest ranges from the source examined. Color in (B) and (D) indicates inter-click intervals (ICI), with buzz starting at 13 ms (Wisniewska et al., 2012). Buzz- and regular-click datasets in (D), used at short- and long-ranges, respectively, have different distributions, but similar medians, because during buzzes the animal repeatedly changed its beamwidth (Figure 6). Beam of the long-range clicks varied less and is better approximated by the median. https://doi.org/10.7554/eLife.05651.006 We therefore experiment two to the beamwidth at close target ranges using a hydrophone array. of the three porpoises, Freja, was to approach a target by a star-shaped array of 48 hydrophones in two (Video 2). the hydrophones were at increasing intervals from the array to the extent of the beam at relatively long ranges while more resolution the target at short ranges Figure 4—figure supplement We then the experiment using an array of spaced hydrophones Figure 4—figure supplement and the target in front of the array, to signal intensity resolution at short ranges. Video 2 Download asset This video cannot be played in place because your browser does support HTML5 video. You may still download the video for offline viewing. Download as MPEG-4 Download as WebM Download as Ogg A representative trial from experiment Video shows a blindfolded porpoise closing on an aluminum target in front of a hydrophone array. The sequence was recorded in a that with the array to m on either side of the centre hydrophone and the target to 0.4 m from array Only clicks recorded when the porpoise was m from the array, at an angle of to its centre and with acoustic axis within cm from the centre hydrophone were for the beamwidth The was with from the by the porpoise. Figure with 1 supplement see Download asset Open asset dB beamwidth variation with indicate beamwidth estimates based on the while the vertical show the the (see in Figure 4—figure supplement 1). Data were gathered with star-shaped arrays in two (Figure and Figure 4—figure supplement large N = and small N = Color indicates the associated with the Only with were considered in the and presented in Figure from the sound source to the of the was We recorded trials with the long-range and trials with the Only trials in which the porpoise swam directly the target and from the and repeatedly its beam over the hydrophone were This in trials for the and trials for the array configuration. For recorded the energy levels at the hydrophones were to the beam pattern of a (Au et al., et al., Only beamwidth estimates based on with (see Figure 4—figure supplement were considered in the a total of and clicks for the and array, respectively. The of this experiment show that the porpoise could its beamwidth in when to a buzz (ICI ≤13 ms; [Wisniewska et al., 2012]) at short target ranges (Figure from a mean beamwidth (i.e., the angle at which the sound energy has by 3 dB relative to the of to a of = = In this way the animal increased the ensonified area ahead of it by up to three times in the terminal buzz phase of its approach to a as indicated by the of the area at a given target range to the area for that range based on the dB beam angle for long ranges (i.e., area the porpoise not to Figure A between the beamwidth of the clicks and distance they were emitted from the target was found for data from experiment = = = = Data from experiment two were also using (see and The three using beamwidth with respect to distance to target = clicks in the with the beamwidths were emitted to the target than clicks in the with the beamwidths Figure 5 Download asset Open asset Beam can triple the ensonified (A) detection volume for a harbour porpoise tracking fish in a based on the sonar and source energy levels as detection et al., of dB 1 and target of dB for the of cm (Au et al., is of the beam is based on beamwidth estimates obtained at short target ranges. The narrow beam is based on the at long range, beam pattern the porpoise not to (B) change in the size of ensonified area ahead of the porpoise as it a target. area was as of a with to target range and an angle corresponding to the dB beam angle in A) or dB beam angle for long ranges in Color indicates inter-click and data points obtained with the large (N = 34) and small (N = 458) array, respectively. The horizontal indicates points where the and the are The of these changes (Figure shows that the porpoise varied the width of its beam within the buzz independently of the inter-click intervals with both narrow and beam angles used at the ICIs (Figure the short- and long-range datasets have different distributions, but similar and the long-range clicks are better by the mean beamwidth (Figure The click frequency by about at the of a buzz (from a long-range of to a of see the color scale in Figure and Figure supplement 1). Figure with 1 supplement see Download asset Open asset variation in beamwidth within the terminal buzz. changes in terminal of two trials (A, C) and their inter-click intervals D). of in (A, C) to beamwidth at long ranges The porpoise used different beamwidths ICIs and Both trials were recorded with the small star-shaped array (light blue in Figure but during the trial in (C, D) the porpoise was not Only data for clicks fulfilling inclusion are This in frequency cannot explain the large changes in beamwidth (Figure supplement between frequency and = = the animal the size of the effective likely by rapid deformations of the melon (Video the of the phonic lips and/or the size and of the associated air To visualize the musculature the melon, we obtained magnetic resonance imaging (MRI) on a dead harbour porpoise. The images nasal that a richly innervated et al., network of facial muscles (Figure 1). These muscles are to the muscles to facial in and and changes in the shape of nasal and their associated air et al., 2009). Video 3 Download asset This video cannot be played in place because your browser does support HTML5 video. You may still download the video for offline viewing. Download as MPEG-4 Download as WebM Download as Ogg porpoises can their melon while producing Video shows a harbour porpoise echolocation click during a It has been by a of two and with the output of a porpoise click The porpoise the melon as it to high repetition rate click changes in the nasal complex can the of sound in the forehead et al., 2008; et al., 2008; Huggenberger et al., to change the field of view. of Discussion Here, we show that harbour porpoises can broaden their biosonar beams in the phase of target approach (Figure unlike echolocating bats, that they are also able to change their beamwidth within the terminal buzz (Figure 6). its the beamwidth from in experiment two to more than in experiment one. A of factors may have to this variability (i) in effective angular resolution (EAR) between the linear array and the star-shaped array, (ii) in the animals' when approaching a fish a aluminum higher from the large array behind the target and the porpoise to use a narrower beam. Porpoises can adjust their buzz clicking rate to prey range when following a fish in open water than when tracking one in the cluttered and more space close to the sea floor (Figure 2). The porpoise and experimental the most likely for the observed between the two This is the to of a whale its acoustic FOV while actively approaching a target. This control is independently of (Figure and Figure supplement 1), by changing the of the melon (Figure et al., the of the phonic lips (Cranford et al., 2014) and the size and shape of the associated air (Aroyan et al., to its structure and et al., the melon has long been considered an acoustic that the and energy loss at the and and that directionality in the emitted click (Au et al., Porpoises have a complex facial musculature (Figure with with times more than facial muscles and to the that deformations of the nasal such as the melon may means to change the FOV et al., 2009). acoustic and observations support that hypothesis by demonstrating that the melon and as the of an