William A. Searcy, Ph.D. - US grants

NONTECHNICAL SUMMARY Nowicki & Searcy, IBN 9408360, Perception, Function and Development of Complex Vocal Signals Animal communication plays an important role in many biologically critical arenas, particularly social behavior, including territorial defense and the attraction and choice of a mate. Bird song is one of the most spectacular cases on this type of behavior, and much of what has been learned about the development and evolution of animal communication has been the result of studies of bird song. In this research project, Dr. Searcy will investigate several aspects of a common characteristic of bird song, different song types. In many songbirds, the males sing variable songs which can be classified into a small number of song types. For example, male song sparrows sing five to thirteen different song types each. This pattern is found in many species but little is known about either how such variability in song develops in the individual or about how it functions in an evolutionary sense. A series of experiments conducted in both the laboratory and the field will investigate: (1) the abilities of song sparrows to discriminate variation both within and between song types; (2) the ways in which such variation contributes toward either attracting a mate or discouraging other territorial males: (3) the extent to which song sparrows differ in the amount of variability in their songs in different regions of the country; and (4) the role of learning and cultural transmission in the development of song type variability. Taken together, the results of these studies will advance the understanding of the evolution and development of animal communication.

Drs. Nowicki and Searcy propose to test whether early nutrition affects the
development of song in birds. Song development and production are controlled in
songbirds by a series of well defined brain areas, which develop to a large
extent during the first two months after hatching. In many species, the details
of song are learned during this same two month interval. Nowicki and Searcy
hypothesize that nutrition during this period affects the development of the
song control regions in the brain and consequently affects song learning. As a
test, they will manipulate level of nutrition in hand-reared sparrows during the
first three weeks post-hatching. The sparrows will be tutored with
tape-recorded songs, and the songs produced by these birds as adults will be
recorded. The stressed and unstressed groups will be compared for the quality
of learning, in terms of how faithfully they have copied the notes of the tutor
songs, and for the quantity of learning, in terms of how many songs are learned
per individual. The brains of the two groups will also be compared, for the
size of the song control regions and the density of neurons in those regions.
Finally, the songs of stressed and unstressed birds will be compared in terms of
how well they function on ecologically relevant tasks.

The idea that stress early in life affects brain development and hence learning
ability is applicable to a wide variety of organisms, from birds to humans.
Song in songbirds provides an excellent model system for studying such effects,
in that the neural control, development, and ecological function of the behavior
are all relatively well known. The study will use this system to enhance our
understanding of the effects of nutrition on the development of complex
behaviors.

Under this US-Brazil-Canada dissertation enhancement research award, Sarah M. Stai, under the sponsorship of William A. Searcy of the University of Miami, will work with Regina H. F. Macedo of the University of Brasilia in Brazil and Frank Rohwer at the Delta Waterfowl and Wetlands Research Station in Portage la Prairie in Canada. They will study the promiscuity and sperm competition in Muscovy ducks. This project has three objectives: 1) to characterize male-female associative patterns through behavioral observations and to estimate the number of mates through DNA analysis; 2) to explore why this species is an exception to the rule of monogamy in waterfowl through cost-benefit analysis, a comparative approach, and hypothesis testing; and 3) to test the passive sperm loss model, a proposed mechanism for sperm competition.

The elucidation of the adaptive significance of promiscuity and an ability to predict the outcome of sperm competition will lead to a better understanding of Muscovy duck reproductive strategies and of mating system evolution in waterfowl. The field research will be done in Brazil and the captive research will be done in Canada. This project will provide benefits to research, teaching, and wildlife management and conservation.

Collaborative research: Developmental and receiver-dependent costs of avian signals.

Stephen Nowicki & William A. Searcy

A central question in the study of animal communication is why signals provide reliable information, especially in cases where the signaler has different interests from the receiver. Theory suggests that signals may be reliable if they are in some way costly. The proposed research applies this theory to a well studied signaling system, birdsong.
Female songbirds use male song to judge the quality of prospective mates. The "nutritional stress hypothesis" proposes that the costs of song development produce a reliable link between a male's song and his quality as a mate. Because song development is costly, any male experiencing an early stress such as food shortage will produce both poor song and a poor overall phenotype, making song quality a reliable measure of overall quality. Previous work has shown that early nutritional stress has a negative impact on the development of the brain areas that control song, on the ability of males to learn songs, and on other aspects of adult phenotype such as body size. The proposed research will extend this work in three ways. First, it will test whether early nutritional stress affects a male's vocal performance, that is his ability to sing songs that are physically challenging to produce. Second, the research will test whether early stress affects the quality of the immune system of adult birds, a trait that should be of special interest to females. Third, the research will ask whether early stress also affects the development of song preferences in females.
Song also serves as an aggressive signal between competing males. In this context, signal reliability may be maintained by costs imposed by the aggressive response of receivers. Signals can reliably predict escalation if those signals also elicit the most aggressive response by receivers. Previous work shows that "soft songs" (songs produced very quietly) reliably predict aggression on the part of the signaler. The proposed research will test whether soft song also is likely to provoke an aggressive response from receivers, as theory suggests. Second, research will test whether soft song reduces the ability of third party individuals to gain information from an interaction. Third, the proposed research will investigate how patterns of signal matching contribute to signaling in aggressive interactions.
The proposed research integrates theory and data concerning animal signaling systems and mate choice with testable hypotheses about the development of brain and behavior. This area has proven to be an effective platform for recruiting and training women and minority scientists, and for disseminating the process of how science is done to the general public. An interactive website will be developed to allow students in grades 6-12 to simulate playback and learning experiments with songbirds.

Male songbirds use a variety of specialized singing behaviors when they interact. These behaviors are presumed to function as signals in male-male competition, yet for many behaviors it remains unclear what information the display is signaling. Examining how male birds perceive and respond to these behaviors is key to understanding how song functions in this context. Song perception by male birds is usually tested by measuring aggressive responses to song playback. The results of such tests are difficult to interpret, because the strongest aggressive response may be given to either the most threatening stimuli or to the least threatening stimuli. This project will use the cardiac response (change in heart rate) evoked by song playback as an alternative measure of the perception of song and other stimuli by male song sparrows. Specifically, this measure will be used to test the perception of low-amplitude song ('soft song'), a singing behavior that is thought to be highly aggressive, and to determine the distance over which soft song can be perceived by birds on their territories. Cardiac measures have proven useful for examining signal perception in a variety of species and contexts, but have not been applied to hypotheses about aggressive signal perception in birds.

Broader Impacts: The broader impacts of this project include promoting the professional development of women in science, and providing opportunities for undergraduate students to gain research skills and experience. Numerous undergraduates and graduates have been mentored in this program, many of whom have gone on to professional careers in animal behavior.

This research will examine associations between communication signals and cognitive ability in two species of songbirds. Song in these species is learned: males memorize external models early in life, and then use these memories to shape their own production when they begin to sing many months later. Because song development involves learning and memory, it is logical to hypothesize an association between song and other aspects of cognition. To test that hypothesis, cognitive ability will be measured in a series of laboratory tasks, for example a novel motor task, in which subjects learn to remove lids from the wells of a foraging grid to obtain food, a color association task, in which subjects learn to associate food with lids of a particular color, and a spatial task, in which subjects learn that food can be found only in certain locations. These cognitive measures will then be related to aspects of song that are the outcome of learning, such as the accuracy with which song models are copied during development and the frequency of sharing of song types with others in the local population. Vocal learning in songbirds shows a series of striking parallels with speech development in humans, and therefore results on the tie between vocal development and cognition in songbirds will have implications for the relationship between cognition and speech in humans. Results from the study will be disseminated not only in scientific outlets but also in workshops for high school biology teachers designed to demonstrate how the study of animal behavior can be used to teach the scientific method.

Although evolution by natural selection has often been depicted as favoring ruthless, selfish behavior, cooperation is actually widespread in nature. Consequently, the evolution of cooperative behavior has become a central problem in biology. The present research examines the evolution of a particular form of cooperation, cooperative nest building in an African bird. Communal nests represent a public goods dilemma: each individual benefits directly from the communal nest, but would benefit more if it could refrain from contributing to nest-building as long as others continued to maintain the nest. Such public goods dilemmas are common in human societies but have rarely been explored in non-human animals.

This research will investigate cooperative nest construction behavior of a Namibian bird, the sociable weaver. Observations of nest construction in nature will examine relative contributions of the sexes and of individuals to test whether cooperation in this instance can be explained via kin selection. Simply, kin selection is a type of natural selection favoring aid to genetic relatives. An agent-based model will be used to further explore the possibility that cooperative nest building can be sustained through kin selection. The computer code used to implement the model will be made available to other scientists, thus facilitating future modeling efforts in social evolution.

In addition, an experiment will test whether individuals that forego cooperative nest construction are punished by others; such punishment is a common explanation for contribution to public goods in human societies. Thus the research will test whether theories explaining contribution to public goods in human societies explain cooperation in this model system. The project will also contribute to the development of the next generation of scientists and engineers. The project includes undergraduate mentoring and training in genetic analyses and behavioral observation, thus providing useful research experience for the next generation of American scientists.

Many animals communicate vocally according to a set of rules. In human conversation for example, individuals avoid overlapping each other, a rule known as "turn taking." Another rule in human conversation, "pair adjacency," dictates that certain responses should follow certain utterances: a greeting should be answered by another greeting, for example, and a question should be followed by an answer. Human conversation is difficult to study because of its complexity, and therefore a need has been recognized for interdisciplinary studies that investigate interaction rules in simpler animal models. This study will address potential biological examples of both turn taking and pair adjacency in a duetting Neotropical bird: the plain wren. This study will be one of the first to address experimentally the development of song in a duetting species and the first to address experimentally the development of the interaction rules that govern duets. Furthermore, this study will support the education of local field guides as well as both Latin and American undergraduates by recruiting them for laboratory and field work.

Mated pairs in various songbirds sing together to produce duets. In some species, including the plain wren, the male and female of a pair alternate their songs so rapidly and precisely that it sounds as if a single individual is singing. In many species that duet, again including the plain wren, males and females have repertoires of sex-specific song elements and follow a "duet code" that specifies which syllable of one sex is used to answer a particular syllable from the other sex. This research will provide the first thorough study of how aspects of duets such as precise temporal coordination, sex-specific elements, and duet codes develop. Plain wrens will be hand-reared in captivity and tutored either with duets and solo songs or with solo songs only. This experiment will answer four main questions: 1) Do plain wrens need experience of duet singing during early development to be able to duet with temporal precision? 2) Do plain wrens have an innate predisposition to learn their own sex-specific songs? 3) Are duet codes learned from duets heard during the early stages of life? 4) Can duet codes be altered after individuals have reached adulthood? A list of published material and primary data available upon request will be posted on the Principal Investigator's laboratory website (http://www.bio.miami.edu/searcylab/karla.html) after publication.