Animals communicate using a spectacular diversity of signals, and these signals are often complex and multifaceted. For example, many insects communicate using a combination of bright colors, sounds, vibrations and pheromones, and the insects may alter these signals in different environmental and social conditions. The broad goal of my research is to understand the functional and mechanistic conditions that favor this kind of complexity in animal signaling, and the consequences of this complexity on signal evolution. My research has focused on studying birds in the wild, and to this end, I have developed techniques for detailed observation and experimental manipulation of both visual and acoustic signals in the field. Below I describe my three current research projects on songbirds and sage-grouse, and my past research on bowerbirds. To see explanations of the images below, hold your cursor over the photo or click on the image.
Studies of animal communication have examined how acoustic signals are adapted to their social function, their ecological context and the physiology of the communicating animals. An important aspect of acoustic communication has been largely left out of these studies -- the directionality of acoustic radiation -- because measuring directionality has proved extremely difficult. A vocalization is considered directional if radiating sound waves have different amplitudes (i.e. loudness) around the animal. The handful of successful studies reveal a large degree of variation in directionality across calls and across species. Though directionality can have dramatic effects on the transmission of acoustic information, we know almost nothing about how directionality varies with signal function, sender morphology and behavior, and the environment in which the signal is transmitted. This is an important gap in our current understanding of acoustic communication, with relevance to the broader issue of how traits, such as communication signals, are shaped by functional necessity and mechanistic constraint.
I am examining the directionality of acoustic communication in passerines. I collaborated with Jack Bradbury and Marc Dantzker at the Cornell Laboratory of Ornithology to develop an acoustic directionality measurement (ADM) system that combines digital audio and video recording with techniques for data analysis and visualization using MATLAB. The ADM system measures amplitude simultaneously on eight microphones arrayed around vocalizing animals in the field, allowing the reconstruction of acoustic radiation patterns in the horizontal plane. The broad goal of this research is to test the hypothesis that the directionality of a vocalization is affected by the social and ecological context of the call, and by the morphology and behavior of the calling animal. We began fieldwork for this project at a field site near Cornell using red-winged blackbirds (Agelaius phoeniceus) as a model species. We measured the directionality of vocalizations from territorial males, and found that directionality varies dramatically among call types, and that the call types with the highest potential cost of eavesdropping are the most directional. Our results also indicate that visual displays accompanying song in redwings can affect acoustic radiation, suggesting an interaction between multiple sexually-selected display traits. I plan to establish a field site in California to continue work on this species at UC Davis. The ADM system can be adapted to study many different species of birds -- as well as insects, anurans and mammals -- so there are many opportunities for future research projects that utilize this system. Click here to see an animated plot of the radiation of a song in red-winged blackbirds.
In addition to studies of acoustic directionality in passerines, postdoc Alan Krakauer and I will use the ADM system to study sexual selection in greater sage-grouse (Centrocercus urophasianus). The spring breeding displays of sage-grouse place them among the most spectacular (and bizarre) birds in the world (click here for video of displaying males). Previous studies of sage-grouse provided indirect evidence that the amplitude of male acoustic displays influences female choice (Dantzker et al., 1999, PDF). However this hypothesis could not be directly tested because amplitude was extremely difficult to measure reliably on a sufficient sample of birds. This previous research gives us good reason to believe that amplitude is important in sexual selection, but we don't yet know how important or why. With the ADM system, we will test the hypothesis that amplitude affects female choice and explore the implications of amplitude on sexual selection.
Because amplitude is affected by directionality and environmental propagation, males will have difficulty sending high amplitude sounds to females, and females will have difficulty comparing amplitude among males; this may lead to adaptations in both sexes to increase benefits during mate choice. Indeed, Dantzker et al. (1999, PDF) found that male displays are highly directional and beamed laterally from the vocal sacs, and that males position themselves lateral to observing females so that the loudest sounds are likely directed at them. In addition, the directionality of male displays is highly variable over time and among males. Using a 24-microphhone recording array as an ADM system, Alan and I plan to examine whether males adjust their acoustic radiation patterns to direct the energy of their displays toward females, and whether variation in directionality affects male courtship success.
Since females often move during courtship, we will examine the degree to which males adjust their positions and/or acoustic radiation patterns to track females, and whether the ability to do so affects male courtship success. To examine this experimentally, Alan and I collaborated with Tom Fowler of the Cornell Lab of Ornithology to build a robotic female sage-grouse that will allow us to measure each male’s ability to track moving females and respond to female behaviors by adjusting their displays. The robot is equipped with a microphone and video camera, allowing us to quantify the male's display from the perspective of the receiving female. Using the ADM system to measure the signal that the male radiates in all directions, and the robot to measure the signal received by the target female, we will have a unique ability to quantify how directionality shapes male display behaviors and female choice in sage-grouse. We began using the robot in experiments in the spring of 2007 near Lander, Wyoming. Click here to see a robot demo and video clip from the fembot spycam. Click here to see video clips featuring the robot by the Sacramento Bee, Science Nation and PBS Nature.
In addition to measuring directionality, our 24-microphone array (pictured left) can be used to locate the males on the lek. Each time a male vocalizes, we can measure the time delay of the sound reaching each of the microphones and use this data to triangulate the male's position to within 0.5 meters. Using these location data, we can create detailed maps of male territories, and examine male vocal interactions along territory boundaries. We can also accurately pinpoint the male's location relative to the robotic female. This is an exciting new technology with great promise for studies of animal ecology, since it allows non-invasive monitoring of animal movements. For localizations, we are using the freeware program Syrinx and custom software developed by Dr. John Burt from the University of Washington.
The complex acoustic displays of sage-grouse and many other galliformes are accompanied by equally complex and striking visual displays. In the future, I hope to expand this research on acoustic displays to include detailed analysis of the morphological and behavioral displays used in courtship. Previous research on sage-grouse has found that only the acoustic components of male displays (as well as time spent displaying and display rate) correlate with male success in mating. I hope that by examining the interactions among male traits, and the ability of males to adjust their displays according to changing environmental and social conditions, that more insight can be gained into the evolution of complex and multifaceted sexual displays found in grouse and in many other animals.
Populations of sage-grouse are declining throughout Wyoming and throughout their range. Grad student Jessica Blickley, Postdocs Stacie Hooper, Sean Hanser and Diane Blackwood and I have been working with the Bureau of Land Management to investigate whether noise from energy development, particularly natural gas and coal bed methane extraction, is contributing to this decline by interfering with acoustic communication on the lek. This project involves three parts:
1) Descriptive Acoustics: We will characterize the major sound sources associated with energy development (e.g. compressors, drilling rigs, road noise). We will better characterize the sound produced by individual sage-grouse and groups of sage-grouse on leks. We will examine how sound propagates through the environment over short (≤50 meters) and long (0.1-5 km) distances over a variety of ground types, vegetation types, and terrains. Sound measurement are made with Automatic Recording Units (ARUs), which can be programed to sample sounds at designated intervals throughout the day, and with a hand-held SPL meter.
2) Experimental: Once noise sources are characterized, we will conduct a series of experiments investigate how grouse respond to controlled noise placed at different distances from their leks.
3) Theoretical: We will develop a landscape-level model of the potential effects of noise from energy development on sage-grouse; this model will allow managers to predict how different sound sources at given locations will affect grouse breeding behaviors.
Fieldwork for this project is being conducted near Pinedale, Wyoming where there is a substantial amount of energy development, and near Lander, where the grouse are still relatively undisturbed. Fieldwork for this project began in spring of 2005 and will continue through spring 2010.
Sexual signaling in bowerbirds
My dissertation research addressed sexual selection and the interaction between males and females during courtship in satin bowerbirds (Ptilonorhynchus violaceus). This work was conducted at the University of Maryland, College Park in collaboration with my dissertation advisor, Gerald Borgia, and my colleagues Albert Uy and Seth Coleman.
Interactive signaling. The sexually-selected display traits of individual males commonly vary over time, but despite this variability, models of sexual selection generally characterize males as having a single trait value. Thus, when variation in male traits is detected in empirical studies, it is often viewed as “noise” with little significance in communication, except in making male traits more costly for females to assess. Variation in female behaviors during courtships—especially in polygynous species with no pair-bonding—is often ignored entirely. Using the satin bowerbird as a model system, I examined both male and female behaviors during courtship, with the goal of explicitly assessing the causes and consequences of within-individual variation in courtship behaviors. My results suggest that variation in male and female behaviors may be due to interactive signaling between the sexes, and that the ability to signal interactively during courtship may itself be a trait favored by sexual selection.
During courtship, male satin bowerbirds must give intense and aggressive courtship displays to be attractive, but these same displays may threaten females, startling them and disrupting courtship. In an analysis of natural courtships, I found that a female behavior (“crouching”) signals the degree of intensity that females will tolerate without being startled—and that females tolerate increasingly intense displays as mate-searching progresses. Thus by giving higher intensity displays as female crouching increases, males can display intensely enough to be attractive without threatening the female with displays more intense than she is ready to tolerate. I tested the hypothesis that male satin bowerbirds reduce the threat of their courtship displays by modulating their display intensity in response to female crouching. To do this, I developed robotic female bowerbirds (see picture, and click here for video), which allowed me to experimentally control crouching and measure male response in the field. I found that males respond to increased female crouching by increasing their display intensity, such that the highest-intensity displays are given when females are less easily threatened. Further, I found that males more effective at modulation startle females less often in natural courtships, improving their courtship success. My results suggest that despite female preference for intensely displaying males, successful males do not always display at maximum intensity, rather, they modulate their intensity in response to female signals. Thus in satin bowerbirds—and in other species where male-female interactions have not yet been examined in detail—sexual selection may favor males with the intrinsic ability to produce attractive displays and the ability to modify them in response to female signals.
Multiple male traits. My dissertation research also addressed the role of multiple male displays in female choice. Males of many species have multiple sexual display traits; there has been a great deal of interest in how multiple male traits evolve, and how they are maintained by sexual selection. To understand the evolution of multiple traits, it is critical to understand how each trait influences female choice. The data from my detailed analysis of male and female courtship behaviors allowed me to address this issue in a unique way—by examining signals and cues given by the female to determine which male display traits are assessed by females during mate choice, and when. I found that females tolerate higher intensity courtship displays from attractive males than from unattractive males—they crouch more for attractive males and startle less during early courtships. This allows attractive males to give higher intensity courtship displays that may further enhance their mating success. I then examined why this is so, finding that male physical display traits (bower decorations) reduce the likelihood that females will be startled. These results suggest that male bower decorations may facilitate the expression of more intense—and thus more attractive—male behavioral displays during courtship. This suggests a novel mechanism by which multiple physical and behavioral traits may interact to influence female choice. Multiple male traits are generally assumed to function independently; these results suggest that by considering interactions among traits, we may gain new insight into the evolution and maintenance of multiple male display traits.
Media coverage of research:
Science Nation video on our sage-grouse studies for the National Science Foundation
Live studio interview about the sage-grouse research on Insight, a Capitol Public Radio (90.9) program (download the Podcast here)
PBS NATURE Special "What Females Want and Males Will Do" featuring the sage-grouse research
National Geographic: http://news.nationalgeographic.com
Quirks & Quarks radio show: http://www.radio.cbc.ca/programs/quirks
Science News magazine: http://www.sciencenews.org
PBS Nature: http://www.pbs.org/wnet/nature
Why Files: http://whyfiles.org/149love/4.html
contact Gail | last updated 3-29-10