Photo: Joseph A. Sisneros
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I am a sensory biologist and acoustician interested in the information content of acoustic signals, and how animals perceive sound. I am also interested in the algorithms used by animals to locate a sound producing object solely via hearing. For my PhD dissertation, I am using the acoustically communicating intertidal nesting toadfish, the plainfin midshipman (Porichthys notatus) as a model to address these broad questions. After spending the winter offshore in deep waters (>100 m), midshipman migrate to rocky intertidal beaches during the summer (May-September) for breeding. Type I or “singing” males nest underneath rocks from which they produce nocturnal, long duration advertisement calls (“hums”) to attract females. These hums are the longest contiguous vocalizations in the animal kingdom! Females localize the nests of humming males in near complete darkness and return to deeper water after spawning. Type I males engage in parental care till the eggs hatch and the fry leave the nest. Type II or sneaker males do not produce hums but rather sneak into the nests of type I males and fertilize a fraction of the eggs. Thus, the midshipman is a great model to answer the following questions:
1) What information do type I males convey to females via their mating hums? 2) How do females perceive the hums? 3) How do females hone in on the location of the humming males? |
Dissertation research
I am pursuing my dissertation in the lab of Dr. Joseph Sisneros, University of Washington Seattle, USA.
Honest acoustic signaling in type I male plainfin midshipman
Type I or "singing" male plainfin midshipman produce mating vocalizations called "hums" which constitute the longest known uninterrupted vocalizations in the animal kingdom. The longest recorded hums have been close to 2 hours in duration. Prior to this study, it was unknown whether the hum contains information about the 'quality' or reproductive potential of the type I male. We recorded the hums of type I males in a laboratory setting and found that the loudness of the hum was positively correlated with body size (body mass and standard length). Harmonic frequencies of the hum increased with body condition up to a threshold beyond which the harmonic frequencies remained relatively constant with improvement in body condition. Larger type I males tend to have greater fitness (father more offspring) in the wild. Females preferred to spawn in the nests of larger males in a laboratory setting. Females were also more attracted to louder hums in sound playback experiments. Our study suggests that females could potentially use loudness to choose the nests of larger males with greater reproductive potential. The harmonic frequencies of the hum have previously been shown to linearly increase with temperature. In our study, we demonstrated that if the temperature is maintained constant, the harmonic frequencies are dependent on body condition, with males in poor condition producing lower harmonic frequencies on average. Therefore, hums of type I males serve as honest indicators of size and body condition.
This study has been published in the Journal of Experimental Biology: Balebail and Sisneros, 2022.
This study has been published in the Journal of Experimental Biology: Balebail and Sisneros, 2022.
Perception of harmonic structure of mating calls in female midshipman
Pitch perception plays an important role in human communication. A key feature of pitch perception is the ability to recognize the harmonic structure of an acoustic signal. The ability to perceive harmonic structure has been documented in mammals, birds, and even some species of frogs. The ecological significance of possessing this perceptual ability, however, remains poorly understood. Perceiving harmonic structure might be adaptive for female plainfin midshipman. Type I or "singing" males produce long duration mating calls ('hums') to attract females for spawning. The hum is like a musical note, possessing a harmonic structure with a fundamental frequency (f0) of 80-120 Hz and several higher harmonic frequencies (all being integral multiples of f0). Midshipman breed in shallow water (< 5 m deep), which functions as a natural high pass filter, allowing only the higher harmonics to propagate long distances. Therefore, perceiving harmonic structure of a hum even when f0 is absent might be crucial for mate call detection and localization in female plainfin midshipman.
We hypothesized that female midshipman can perceive the hum’s harmonic structure even in the absence of f0, and that they possess the ability to discriminate a periodic hum from an aperiodic hum lacking a harmonic structure. To test these hypotheses, we performed two-choice acoustic trapping experiments in the natural rocky intertidal breeding environment of midshipman at Seal Rock, Brinnon, WA, USA during the summers of 2021 and 2022. Acoustic stimuli were relayed during the night through underwater speakers contained inside two fish traps placed 2-4 m apart. The following acoustic stimuli were synthetically generated: an average hum, a hum with diminished f0, and an acoustic signal containing the same f0 as a hum but with scrambled higher harmonic frequencies (aperiodic hum). The number of females captured overnight in each trap represented the attractiveness of the acoustic stimulus. Overall, our results are suggest that the fundamental frequency (f0) is both necessary and sufficient to attract female midshipman, and the harmonic note-like structure is not an important factor in mate attraction. Therefore this species might be highly vulnerable to low frequency anthropogenic sounds in the ocean, which might mask the fundamental frequency. Whether the midshipman or other fish species have the ability to detect the harmonic structure of sounds in general remains an open question. To the best of my knowledge, this study represents the first attempt to study mate call perception in the natural environment in fishes. I am in the process of writing up these results for publication.
We hypothesized that female midshipman can perceive the hum’s harmonic structure even in the absence of f0, and that they possess the ability to discriminate a periodic hum from an aperiodic hum lacking a harmonic structure. To test these hypotheses, we performed two-choice acoustic trapping experiments in the natural rocky intertidal breeding environment of midshipman at Seal Rock, Brinnon, WA, USA during the summers of 2021 and 2022. Acoustic stimuli were relayed during the night through underwater speakers contained inside two fish traps placed 2-4 m apart. The following acoustic stimuli were synthetically generated: an average hum, a hum with diminished f0, and an acoustic signal containing the same f0 as a hum but with scrambled higher harmonic frequencies (aperiodic hum). The number of females captured overnight in each trap represented the attractiveness of the acoustic stimulus. Overall, our results are suggest that the fundamental frequency (f0) is both necessary and sufficient to attract female midshipman, and the harmonic note-like structure is not an important factor in mate attraction. Therefore this species might be highly vulnerable to low frequency anthropogenic sounds in the ocean, which might mask the fundamental frequency. Whether the midshipman or other fish species have the ability to detect the harmonic structure of sounds in general remains an open question. To the best of my knowledge, this study represents the first attempt to study mate call perception in the natural environment in fishes. I am in the process of writing up these results for publication.
Role of the swim bladder in directional hearing
Sound is a mechanical disturbance passing through an elastic medium which causes particles in the medium to vibrate (termed as "particle motion") and also causes local fluctuations in pressure (called "sound pressure"). The ears of terrestrial vertebrates detect sound pressure whereas fishes primarily detect sound via particle motion. When the sound source is a monopole and close to the animal, the position of the source can be computed by triangulating the particle motion vectors at two different points in space. Fish auditory systems have been shown to use vector-sensing to localize sound sources in the near field (At distances much smaller than the wavelength). However, when the sound source is located far away from a fish, there is a 180 degree ambiguity in determining the direction of the sound source via particle motion alone. How do fishes resolve this 180 degree ambiguity in directional hearing? The gas filled swim bladders that many fishes possess allow the detection of sound pressure. When a sound passes through a fish, the hair cells (auditory receptors) in the inner ears are directly activated by particle motion created by the sound source. Due to changes in pressure due to the passage of the sound, the swim bladder expands and contracts, functioning like a secondary sound source, generating particle motion which stimulates the inner ears, thus potentially informing fishes about sound pressure. The phase model has long been proposed as a mechanism to resolve the 180 degree ambiguity in directional hearing in fishes. It predicts that fishes can determine the direction of the sound source by computing the phase relation between sound pressure and particle motion, which changes predictably depending on the direction of the sound source. However, this hypothesis remains largely untested. I am using a numerical modelling technique (finite element analysis, FEA) on a specialized FEA software called COMSOL to test this hypothesis. I am generating 3d models inspired by the the actual shapes of the swim bladder and inner ear bones (otoliths) of female plainfin midshipman, which have been shown to localize the sounds of calling type I males with high accuracy. I am currently simulating how the inner ear bones move in response to monopole point sources or plane wave sources, in the presence and absence of the swim bladder. To begin with, I am using a simplified model, enclosing the swim bladder and otoliths in a water sphere, assuming that the acoustic properties of fish tissues to be the same as water. In future, these simple models can be expanded to incorporate material properties of bones and even soft tissues, and the activation profiles of the hair cell fields located close to the otoliths.
Natural underwater sounds as sources of information and noise for fishes
Ambient sound is the background sound present in the environment due to all sound sources other than the source of interest. Despite recent increases in anthropogenic sounds in aquatic environments, natural sounds still make up a large component of the ambient sound spectrum. Ray-finned fishes are the most diverse group of vertebrates on the planet. All studied ray-finned fishes possess a functional auditory system. Proponents of the matched filter hypothesis argue that hearing evolved in this group to best detect the vocalizations of conspecifics. However, several fishes do not vocalize and sound production is likely not an ancestral trait, but evolved independently several times in fishes. Richard Fay (2009) in his review 'Soundscapes and the sense of hearing of fishes' suggested that ambient sound, rather than acting as noise, contains information about the surrounding environment and auditory systems of fishes have evolved to sense and interpret this information. Studying how fishes extract information from natural sounds are essential for determining how rise in anthropogenic noise due to human activities can disrupt this information and thereby affect the long-term survival of fishes. Additionally, studying how fishes have evolved to cope with natural sources of noise may provide insights into the types of anthropogenic noise which fishes are most vulnerable to as well as types of noise which are inconsequential to survival and reproduction. We are in the process of writing a review paper to submit to the International Conference for the Effects of Noise on Aquatic Life 2022, where we highlight the major natural sources of ambient sound and their potential to function both as sources of information and noise for fishes. We summarize known literature on how fishes use sounds as cues for important behaviors. We also document instances where natural sounds interfere with the detection of relevant cues and signals. While there is evidence that fishes extract information about the environment from natural sounds, and that natural sounds can function as noise, data on the effect of natural sounds and soundscapes on the physiology and behavior of fishes is limited. Such studies are urgently required because the window for collecting this body of knowledge is fast disappearing with rising anthropophony in aquatic environments.
Past research
Landing maneuvers of houseflies (Musca domestica) on vertical and inverted surfaces (Master's project)
I did my master's research in the lab of Dr. Sanjay Sane, National Centre for biological Sciences, Bengaluru, India.
Insects can land on substrates having different orientations and textures. High speed videos of insect landings have revealed that landing maneuvers are complex behaviors which can be decomposed into sequences of modules, like body-deceleration, leg-extension, and body rotations. Despite the complexity of the maneuver, landings are performed quite quickly, within a fraction of a second. Prior to our study, it was unknown if insects use similar or different 'rules' or algorithms to land on substrates oriented in different directions. We conducted a series of experiments in which houseflies (Musca domestica) were lured to land on vertical or inverted surfaces. Their landing trajectories were recorded with multiple highspeed cameras filming at 3000-4000 fps. We observed that well-controlled landings occurred on both surfaces when the distance at which flies began slowing down was proportional to the component of flight velocity perpendicular to the direction of the landing surface. The ratio of distance from the landing surface to velocity at the onset of deceleration (called 'tau' or 'time to collision') was conserved, despite substantial differences in the mechanics of vertical and inverted landings. Flies which did not begin slowing down at this value of tau bumped their head against the landing surface, suggesting that these landings were less controlled. Flies also extended their legs before touchdown. Unlike deceleration, leg-extension was independent of approach velocity or how far the flies were from the landing surface. Thus, the robust reflexive visual initiation of deceleration is independent of substrate orientation, and combines with a more variable initiation of leg-extension. Together, these combinations of behaviors likely enable flies to land in a versatile manner on substrates of various orientations. The simple landing algorithms that we have uncovered could be utilized to guide landings in human made flying objects.
This study was published in Plos One: Balebail et al., 2019.
Insects can land on substrates having different orientations and textures. High speed videos of insect landings have revealed that landing maneuvers are complex behaviors which can be decomposed into sequences of modules, like body-deceleration, leg-extension, and body rotations. Despite the complexity of the maneuver, landings are performed quite quickly, within a fraction of a second. Prior to our study, it was unknown if insects use similar or different 'rules' or algorithms to land on substrates oriented in different directions. We conducted a series of experiments in which houseflies (Musca domestica) were lured to land on vertical or inverted surfaces. Their landing trajectories were recorded with multiple highspeed cameras filming at 3000-4000 fps. We observed that well-controlled landings occurred on both surfaces when the distance at which flies began slowing down was proportional to the component of flight velocity perpendicular to the direction of the landing surface. The ratio of distance from the landing surface to velocity at the onset of deceleration (called 'tau' or 'time to collision') was conserved, despite substantial differences in the mechanics of vertical and inverted landings. Flies which did not begin slowing down at this value of tau bumped their head against the landing surface, suggesting that these landings were less controlled. Flies also extended their legs before touchdown. Unlike deceleration, leg-extension was independent of approach velocity or how far the flies were from the landing surface. Thus, the robust reflexive visual initiation of deceleration is independent of substrate orientation, and combines with a more variable initiation of leg-extension. Together, these combinations of behaviors likely enable flies to land in a versatile manner on substrates of various orientations. The simple landing algorithms that we have uncovered could be utilized to guide landings in human made flying objects.
This study was published in Plos One: Balebail et al., 2019.