The Broad-billed Motmot, or Electron platyrhynchum, was one of the species recorded for this study.

The Broad-billed Motmot, or Electron platyrhynchum, was one of the species recorded for this study.

Abstract
Sound with fewer harmonics is believed to be harder for humans to localize. Birds may have evolved calls with fewer harmonics in order to reduce predation risk. In light of this hypothesis, we predicted that bird calls lacking harmonics would be harder to localize. We asked blindfolded human test subjects to localize recorded bird calls with or without harmonics. Contrary to our prediction, birdcalls of certain species were harder to localize with harmonics. However, the dominant frequency and number of harmonic bands in calls also affected subjects’ ability to localize the call. These arboreal birds employ a combination of higher frequencies and harmonics, which may bounce off of the dense foliage, altering predators’ perception of sound.

Introduction
Animals vocalize for a variety of reasons-to warn others about potential predators, to establish and maintain territory boundaries, and to attract mates, among others. Male birds often call to attract mates, but calling also increases predation risk. Cryptic coloring, flocking (1), calling in sheltered areas, and calling for short time periods are adaptations that may lower predation risk. Calls containing fewer harmonics (frequency bands at equal intervals above the dominant frequency band of the call) may also be harder for predators to localize (2). Forest guides and biologists around La Selva biological station, Costa Rica expressed difficulty in localizing the calls of certain bird species, such as Trogons (pers. corr. Kenneth Alforo). We examined the hypothesis that having a call with fewer harmonics decreases predation risk. Since humans and predators of birds both use aural cues to localize birds, the theoretical model predicts that human subjects would experience more difficulty determining the direction of a call with fewer harmonics compared to a call with more harmonics.

A Slaty Tailed Trogon (Trogon massena).
A Slaty Tailed Trogon (Trogon massena).

Methods
We recorded birdcalls on 13 February and conducted experimental trials on 14-15 February, 2010, at La Selva Biological Station, Costa Rica. We recorded the calls of three bird species (Western Slaty-Antshrike (Thamnophilus atrinucha), Broad-billed Motmot (Electron platyrhynchum), and Slaty Tailed Trogon (Trogon massena)), representing a wide range of harmonic characteristics and dominant frequencies, using a 22″ Telinga parabola with a Sennheiser ME62 microphone running on a K6 power module and a Marantz 661 solid state digital recorder sampling at 24 bits and 96 kHz. We also used the pre-recorded call (3) of a Violaceous Trogon (Trogon violaceus), a species often found at La Selva, as we were unable to record one ourselves. Using R statistical programming language and Raven Lite 1.0 Interactive Sound Analysis Software, we altered the calls, removing harmonics from T. atrinucha, E. platyrhynchum, and T. violaceus and adding harmonics to T. massena, which had weak natural harmonics. We standardized volume and duration of all call clips.

We conducted experimental trials in the forest around the Arboleda trail roughly 20 m from the laboratory building at La Selva Biological Station. To test subjects’ ability to localize bird calls, we asked our human subjects (Dartmouth undergraduates and other scientists) to listen blindfolded to bird calls played 8.8 m from the subject in a random direction. We played each manipulated and unmanipulated call once (8 total calls) using an Apple iPodNano connected to Radio Shack fold-up, portable speakers, held over a researcher’s head. We constructed a 360° protractor out of cardboard, and placed it on a pole roughly 0.5 m above the ground. Upon hearing the recorded call, subjects aimed an arrow on the protractor towards the perceived direction of the call. Using a string stretched tightly from the navel of the researcher holding the iPod to the center of the protractor, we measured and recorded the angle between the actual call and the direction indicated by the subject.

Figure 2: The angle between the location of a bird call (A: T.  atrinucha, B: E. platyrhynchim, C: T. Massena, D: T. violaceus) and the  subject's perceived location of the bird call (Degrees Off) of calls  with no harmonics compared to the Degrees Off of calls with harmonics,  with equivalence line shown (n=18).  La Selva Biological Station, Costa  Rica, February 2010.
Figure 2: The angle between the location of a bird call (A: T. atrinucha, B: E. platyrhynchim, C: T. Massena, D: T. violaceus) and the subject’s perceived location of the bird call (Degrees Off) of calls with no harmonics compared to the Degrees Off of calls with harmonics, with equivalence line shown (n=18). La Selva Biological Station, Costa Rica, February 2010.
Figure 1: Spectrograms of calls of four different bird species: T.  atrinuca (1A. Harmonics, 1B. No Harmonics), E. platyrhynchum (1C.  Harmonics, 1D. No Harmonics), T. Massena (1E. Harmonics, 1F. No  Harmonics), and T. violaceus (1G. Harmonics, 1H. No Harmonics). La Selva  Biological Station, Costa Rica, February 2010.
Figure 1: Spectrograms of calls of four different bird species: T. atrinuca (1A. Harmonics, 1B. No Harmonics), E. platyrhynchum (1C. Harmonics, 1D. No Harmonics), T. Massena (1E. Harmonics, 1F. No Harmonics), and T. violaceus (1G. Harmonics, 1H. No Harmonics). La Selva Biological Station, Costa Rica, February 2010.

Results
The natural calls of the four focal bird species had the following number of harmonic bands above the dominant frequency: T. atrinucha 13, T. violaceus 5, E. platyrhynchum 2, T. Massena 0 (Fig. 1). The manipulated calls of T. Massena had two harmonic bands above the dominant frequency, and the manipulated calls of all other species had zero. The dominant frequency of the four species’ calls were: T. atrinucha 1.6 kHz, T. violaceus 1.5 kHz, T. Massena 1.4 kHz, E. platyrhynchim 1 kHz.

T. atrinucha and T. violaceus were more difficult to find with harmonics (Figure 2). Harmonics did not affect people’s ability to locate the calls of E. platyrhynchim (natural harmonics) and T. Massena (added harmonics). Harmonics and the interaction between harmonics and the bird species affected the ability of the test subject to localize the bird call (Table 1). Although there appeared to be no effect of test subject, we observed variability in subjects’ ability to localize calls, which could be due to subjects’ previous acoustic experience. The calls with higher dominant frequencies and a greater number of harmonics tended to be harder to localize (Figures 3 and 4).


Table 1, Figure 3, Figure 4Discussion
Although sounds with more harmonics are believed to be easier to localize, our results suggest that bird calls with more harmonics are actually harder to localize. We hypothesize that this finding is due to an interaction between vegetation density and harmonic structure. The dominant frequency of the call and the number of harmonic bands may also affect how easy it is to localize a bird call: the two bird species calls with a higher dominant frequency and a greater number of harmonic bands (T. atrinucha and T. violaceus) were harder to localize with harmonics than without harmonics. In wooded areas, harmonics and higher frequencies may bounce off vegetation and become distorted, confusing the listener. Comparing the ability to localize bird calls in dense vegetation versus open areas may shed light on this phenomenon.

As a result, harmonics may be an adaptation to decrease predation risk in some bird species. However, for two species we studied (E. platyrhynchum and T. Massena) the presence of harmonics did not affect a person’s ability to localize the call. In these species, female preference for calls with purer tones could exert a stronger selective pressure than predation. Variation in the number and frequency of harmonic bands may also be an example of niche partitioning where acoustic space is a limited resource. Though it is conventionally suggested that harmonics make sound easier to localize (2), environmental factors such as vegetation may alter the perception of sound.

Acknowledgements
Research was conducted under the mentorship of
Laurel Symes and Matt Ayres as a part of the Biology Foreign Study Program.

References

1. G. Page, D. F. Whitacre, The Condor. 77, 73-83 (1975).
2. S. G. Goodridge, Dissertation, North Carolina State University (1997).
3. D. L. Ross, Violaceous trogon. Costa Rican Bird Song Sampler (audio recording). Cornell Laboratory of Ornithology, track 7 (1998).