Charles R. Brown
|-B.A., Austin College
Office: 330D Oliphant Hall
Phone: (918) 631-3943
My research interests center on the evolution of social behavior
in vertebrates. I am especially interested in the effect of group size on social behavior. Much of my research
focuses on why animals live in colonies. The adaptive significance of group-living in animals has attracted the
interest and attention of biologists for decades, and we presently have a relatively clear understanding of the
selective pressures that lead to territoriality (economic defensibility) and cooperative or communal breeding (inclusive
fitness and habitat limitation) in vertebrates. My National Science Foundation-funded long-term research focuses
on a colonially nesting bird, the cliff swallow (Petrochelidon pyrrhonota), which I have been studying at a field
site in Nebraska for the last 21 years.
There are four major aspects to my research program:
of the socio-ecological costs and benefits of coloniality (e.g., predator avoidance, ectoparasitism, enhanced food-finding)
as a function of group size.
(2) Evaluation of
the alternative reproductive options (e.g., conspecific brood parasitism, extra-pair copulations) that become available
to animals once they have formed groups.
of the demographic consequences of living in colonies and in particular the effect group size and associated socio-ecological
costs and benefits may have on life history parameters.
(4) Examination of the observed patterns of colony choice by individuals
and hypotheses for why group size varies.
Cliff swallows are common throughout much of western North America, building their mud nests in dense colonies
underneath rocky overhangs on the sides of cliffs and canyons and also underneath bridges and in highway culverts.
My study site is in southwestern Nebraska near the University of Nebraska's Cedar Point Biological Station. In
this area cliff swallows breed in colonies ranging in size from 2 to 3700 nests, plus solitarily, making this population
ideal for investigating the effects of group size.
(1) The socio-ecological costs and benefits of coloniality
Over the years I have examined a variety of potential costs and benefits of cliff swallow coloniality and how they
vary with group size. This was a major focus of my research program in the early years of studying cliff swallows,
and continues to date. These results are described fully in my book, Coloniality in the Cliff Swallow. Below I
highlight two of the more interesting aspects of this work, some of the novel findings, and the related work planned
or in progress.
swallow colonies function as "information centers" in which individuals unsuccessful at finding food
locate other individuals that have found food and follow them to a food source. Many people had searched for information
centers in various species of birds and mammals since the early 1970's, but I was the first to document their existence
in any bird (Science 234: 83-85, 1986). Advantages associated with information sharing on the whereabouts of food
are substantial and probably represent a major reason why cliff swallows live in colonies (Ecology 69: 602-613,
1988). I also discovered that cliff swallows represent one of the few birds (and indeed non-human vertebrates)
that actively communicate the presence of food to others by giving distinct signals (calls) used only in that context
(Anim. Behav. 42: 551-564, 1991). The evolution of such information sharing is perplexing, because the typical
beneficiaries of calling are individuals unrelated to the caller. Future work is planned to investigate individual
differences in foraging efficiency and potential asymmetries among individuals in the benefits gained from information
sharing; the degree to which cliff swallows forage in a "risk-sensitive" manner; how foraging-related
benefits vary with group size; and how features of the local resource base (that is, differences in prey availability
and type) affect information sharing in colonies of different sizes.
swallows are associated with several blood-sucking ectoparasites, and infestations in the nests of some colonies
can be severe. Ectoparasites increase with cliff swallow colony size and severely depress nestling swallow body
mass and survivorship (Ecology 67: 1206-1218, 1986). My work demonstrated the most substantial, regularly occurring
cost due to parasites for a colonial species yet described. Ectoparasitism undoubtedly represents the most important
cost of living in colonies for cliff swallows. Future work will model the spread of ectoparasites within colonies
of different sizes and spatial configurations, to predict the degree of within- and between-colony variance in
parasite load and how this variance affects the birds' responses. Using the long-term data from my population,
I am charting patterns in annual colony site usage to determine if variation in site usage is an adaptive response
to parasite build-ups. Studies of ectoparasitism are facilitated by our experimental fumigation of nests in the
field, which makes it possible to create parasite-free nests wherever we wish. In collaboration with Bruce Rannala,
I have begun to address the population genetics of one of the ectoparasites, the cimicid swallow bug. Populations
of these bugs occur in discrete colonies with limited dispersal between colony sites. We have begun to test hypotheses
concerning the population structure and differentiation of these bugs using both empirical (field) data and molecular
genetic techniques. In collaboration with scientists at the Centers for Disease Control in Fort Collins, Colorado,
I have also initiated studies of arbovirus transmission within cliff swallow colonies. The cimicid bug is a vector
for western equine encephalitis virus, and presently we are investigating how swallow colony size and density and
a colony's spatial position relative to other colonies influence viral transmission using a metapopulation approach.
This work has obvious biomedical implications.
(2) Alternative reproductive options
Once animals form colonies, opportunity exists for some individuals to exploit others, and these options often
do not exist for more solitary animals. Colonial individuals can parasitize the reproductive effort of others by
laying eggs in neighbors' nests (conspecific brood parasitism). Males may seek copulations with nearby females
to whom they are not paired (extra-pair copulations). With neighboring nests in close proximity, the potential
exists to steal mud and nesting material for one's own use, as well as to perhaps decrease the relative fitness
of neighbors by destroying one or more of their eggs. My research has investigated all of these potential reproductive
options (see book).
Conspecific brood parasitism.-- I was among the first to show (Science 224: 518-519, 1984) that conspecific brood
parasitism is a major strategy used by substantial numbers of individuals; up to 43% of cliff swallow nests may
have one or more eggs not belonging to the owners. Within the last ten years, behavioral ecologists have recognized
the importance of conspecific brood parasitism, and it has now been reported in a variety of bird species. I discovered
a new form of brood parasitism previously unknown in birds (Nature 331: 66-68, 1988). Cliff swallows not only lay
eggs in other individuals' nests but also physically carry eggs into neighboring nests. This novel behavior expands
the time window during which nests may be parasitized, and egg transfer occurs regularly in swallow colonies. I
have used protein electrophoresis to study parentage in cliff swallow broods, and the biochemical analyses have
suggested that brood parasitism is a major alternative strategy used by these birds. I have also determined that
cliff swallows often destroy one or more eggs of their neighbors. Birds furtively enter an unattended neighboring
nest and toss out single eggs. These egg tossings are not related to attempts to usurp nests, and as a result their
adaptive significance is puzzling.
(3) The demographic consequences of coloniality
To fully measure the costs and benefits of coloniality, one must be able to follow individuals throughout their
lifetimes and measure lifetime reproductive success. Cliff swallows can live up to at least eleven years, and thus
annual measures of reproductive success are potentially misleading, especially if success varies in any way with
age, as my data suggest for cliff swallows. One of the major goals in my research thus far has been to mark large
numbers of individuals, enabling me to follow the reproductive histories of these birds. By knowing the histories
of individuals from year to year, I am able to measure lifetime reproductive success; determine whether an individual's
choice of colony size from year to year is stochastic or to any degree predictable; whether kin tend to settle
near each other; whether reproductive costs occur in older individuals; the long-term effects of ectoparasites;
how reproductive success affects colony site fidelity; the effect of colony size on cohort recruitment into the
population; and other questions critical to an understanding of social evolution at the population level.
Since 1982, my assistants and I have marked over 158,000 birds in our study population with permanent bands. Some
information is known for each of these individuals, and many have been caught repeatedly in successive years. I
am now gathering a huge amount of recovery information each year, and my data set is unique. I know of no comparably
sized data set on any North American species that will provide this kind of information.
My long-term mark-recapture program is beginning to yield results. For example, I have found that the extent of
ectoparasitism a nestling bird experiences during the short time it is in the nest (21 days) has a major influence
on whether that individual disperses to another colony the following spring or returns to its natal site (Ecology
73: 1718-1723, 1992). Ectoparasitism thus appears to determine dispersal, a result not previously known for birds
or mammals, and one that has implications for social behavior, population genetic structure, and host-parasite
coevolution. I have begun to apply mark-recapture data to address other life-history questions, such as how survival
is related to clutch size, laying date, and the tendency to engage in conspecific brood parasitism or extra-pair
(4) Why do animals choose colonies the way they do?
Cliff swallows, like most colonial birds, exhibit substantial variation in colony size. Some individuals nest solitarily,
others breed in moderately sized colonies, and still others live in huge colonies of thousands of birds. Colony
size variation has not been explained satisfactorily in general or for any single species. My data are now beginning
to suggest that birds in certain colony sizes are more successful than birds in other colony sizes, yet extensive
size variation persists. I have proposed various hypothesis to explain why birds choose colony sizes in the observed
fashion (Trends Ecology Evolution 5: 398-403, 1990), and have begun to examine these hypotheses in cliff swallows.
I have studied movement patterns of cliff swallows upon their return to the study area and before they have chosen
a colony in which to breed. Birds are caught and radio transmitters affixed to their backs, and their subsequent
movements followed for 7-21 days. Cliff swallows have proven to be easy species to radio-track. Individuals clearly
visit many colony sites before settling; they do not automatically settle in the first one they visit or even the
first one they find a nest in. They select a colony in many cases days before successfully establishing ownership
of a nest. The birds also move extensively between colonies late in the year. These results indicate that the birds
obviously assess sites, but the cues they use are still not clear.
I am also using my extensive long-term data set to examine the histories of the birds' colony choices from year
to year. Payoffs for colonies of certain sizes may vary with age or condition of the bird, and thus birds should
switch between sites as they get older or their condition changes. Cliff swallows move extensively among sites
between years, and the patterns will likely tell us much about the advantages and disadvantages of using certain
colony sizes and how these differ among birds.
(1) Completion of the long-term demographic study. To achieve robust estimates of survival, cohorts must be followed for 3-4 years,
and consequently I anticipate continuing to collect some demographic data through 2001. As we compile enough information
for analyses of the effect of individual years on survival probabilities, this long-term study will be especially
valuable in determining the importance of particular "good" and "bad" years on life history.
For example, 1992 was the third coldest summer in Nebraska on record (dating to 1876). Many cliff swallows died,
and the demographic consequences may persist for years. In 1996, another severe mortality event caused by bad weather
reduced the population by about 50%, and we are now exploring the implications and natural selection that may have
resulted from this event (see Evolution 52: 1461-1475, 1998).
(2) Studies of transmission dynamics of ectoparasites and their
associated alphaviruses. My work to date has indicated that ectoparasitism
is complex in cliff swallows, with unpredictable effects on the birds' behavior and life histories. We have only
scratched the surface in our understanding of host-parasite coevolution in this system. Future work is planned
to investigate, in particular, the between-group and within-group transmission of ectoparasites and their viruses,
work that will have direct relevance to epidemiology. This system also provides an ideal model to study genetic
differentiation among the parasites themselves. Hemipteran swallow bugs, confined almost exclusively to the cliff
swallows' nests in spatially discrete and often isolated colonies, exhibit rather limited dispersal between colonies
and often undergo periods of extinction within a site when the birds choose not to occupy it in a particular year.
The bugs provide a superlative opportunity to test, with both field data and molecular methods, various equilibrium
and non-equilibrium models of genetic differentiation among animals exposed to frequent extinction and occasional
recolonization events. I am presently collaborating with others (and plan to continue to do so) whose primary interest
is in population genetic questions. We have initiated research to understand the transmission mechanisms that produce
the observed increase in parasitism by swallow bugs with cliff swallow group size. Experiments will measure the
rate at which bugs immigrate into a colony and the rate at which transient cliff swallows (that introduce bugs)
visit different colonies. The results will be among the first attempts to measure between-group transmission of
parasites in a social species. The swallow bug also serves as a vector for arthropod-borne alphaviruses (genus
Alphavirus) that are closely related to those that cause western equine encephalitis. In cooperation with virologists
at the Centers for Disease Control, we are studying the prevalence and transmission dynamics of encephalitis-related
alphaviruses in cliff swallow colonies. Preliminary results show several as yet unidentified virus strains isolated
from swallow bugs, and we have found an increased incidence of virus in nests in larger colonies. We are studying
the transmission cycle and ecology of the viruses associated with cliff swallows and their ectoparasites; this
system can provide a model for the study of other Alphavirus involving migratory birds.
(3) Information centers.
We have only begun to understand the complexities of information sharing in these birds. There is evidence now
that some individuals within a cliff swallow colony forage in very different ways than others. How do these foraging
strategies lead to the overall patterns of information sharing seen in cliff swallow colonies?
(4) Comparisons with cave swallows.
I am initiating a comparative study of the related cave swallow (Petrochelidon fulva), which occurs in Central
America, Mexico, and the southwestern United States. To date my work has focused almost exclusively on a single
species (cliff swallow), but comparisons with the cave swallow are likely to be instructive. For example, cave
swallows are intermediate between highly colonial cliff swallows and more solitary barn swallows (Hirundo rustica)
in virtually all aspects of their breeding biology and social behavior. Barn swallows live in colonies because
their nesting substrates are limited, while cliff swallows clearly do not live in colonies for that reason. Cave
swallows may reveal what ecological or social pressures have brought about the transition to a more social life
style. Involvement of graduate students in this seems likely.
(5) Hormonal and immunological correlates of colony size. In collaboration with others, I have initiated a comparative study of hormone levels
among cliff swallows in different sized colonies. A bird's hormone condition may reflect its social environment,
with serious consequences for its immunocompetence which in turn may affect its survival and lifetime reproductive
success. A bird's hormone levels may also cause it to choose a given colony size. I have also begun a comparative
study of immunocompetence among cliff swallows in different sized colonies. Immunocompetence is a measure of condition
in birds, and this study should help reveal what sort of individual ("quality") differences occur among
birds occupying small versus large colonies. We will also explore the hypothesized connections between hormone
levels and immunocompetence.
- Biol 3153-Animal Behavior
- Biol 3164-Field Ecology
- Biol 3614-Ornithology
- Brown, C. R., M. B. Brown, S. A. Raouf, L. C. Smith, and J. C. Wingfield.
2005. Effects of endogenous steroid hormone levels on annual survival in cliff swallows. Ecology, in press.
- Smith, L. C., S. A. Raouf, M. B. Brown, J. C. Wingfield, and C. R. Brown.
2005. Testosterone and group size in cliff swallows: testing the “challenge hypothesis” in a colonial bird.
Hormones and Behavior 47: 76-82.
- Brown, C. R., and M. B. Brown. 2004. Group size and ectoparasitism affect
daily survival probability in a colonial bird. Behavioral Ecology and Sociobiology 56: 498-511.
- Brown, C. R., and M. B. Brown. 2004. Empirical measurement of parasite
transmission between groups in a colonial bird. Ecology 85: 1619-1626.
- Brown, C. R., and M. B. Brown. 2003. Testis size increases with colony
size in cliff swallows. Behavioral Ecology 14: 569-575.
- Brown, C. R., R. Covas, M. D. Anderson, and M. B. Brown. 2003. Multistate
estimates of survival and movement in relation to colony size in the sociable weaver. Behavioral Ecology 14: 463-471.
- Brown, C. R., and M. B. Brown. 2002. Spleen volume varies with colony
size and parasite load in a colonial bird. Proceedings of the Royal Society of London B 269: 1367-1373.
- Brown, C. R., N. Komar, S. B. Quick, R. A. Sethi, N. A. Panella, M. B.
Brown, and M. Pfeffer. 2001. Arbovirus infection increases with group size. Proceedings of the Royal Society of
London B 268: 1833-1840.
- Møller, A. P., S. Merino, C. R. Brown, and R. J. Robertson. 2001.
Immune defense and host sociality: a comparative study of swallows and martins. American
Naturalist 158: 136-145.
- Brown, C. R., and M. B. Brown. 2001. Avian coloniality: progress and problems.
Pp. 1-82 in Current Ornithology,
Vol. 16 (V. Nolan and C. F. Thompson, eds.). Plenum, New York.
- Brown, C. R., and M. B. Brown. 2000. Heritable basis for choice of group
size in a colonial bird. Proceedings of the National Academy of Sciences USA 97: 14825-14830.
- Brown, C. R., M. B. Brown, and E. Danchin, 2000. Breeding habitat selection
in cliff swallows: the effect of conspecific reproductive success on colony choice. Journal
of Animal Ecology 69:133-142.
- Brown, C. R., and M. B. Brown, 2000. Nest spacing in relation to settlement
time in colonial cliff swallows. Animal Behaviour 59:47-55.
- Brown, C. R., and M. B. Brown, 1999. Natural selection on tail and bill
morphology in barn swallows Hirundo rustica during severe weather. Ibis 141:652-659.
- Brown, C. R., and M. B. Brown, 1999. Fitness components associated with
laying date in the cliff swallow. Condor 101:230-245.
- Brown, C. R., and M. B. Brown, 1999. Fitness components associated with
clutch size in cliff swallows. Auk
- Brown, C. R., and M. B. Brown, 1998. Intense natural selection on body
size and wing and tail asymmetry in cliff swallows during severe weather. Evolution 52:1461-1475.
- Brown, C. R., and M. B. Brown. 1998. Fitness components associated with
alternative reproductive tactics in cliff swallows. Behavioral Ecology 9:158-171.
- Brown, C. R. 1998. Swallow
Summer. Univ. Nebraska Press, Lincoln, 371 pp.
- Brown, C. R. and M. B. Brown, 1996. Coloniality
in the Cliff Swallow: the Effect of Group Size on Social Behavior.
Univ. Chicago Press, Chicago, 566 pp.
- Brown, C. R. and M. B. Brown, 1988. A new form of reproductive parasitism
in cliff swallows. Nature 331: 66-68.
- Brown, C. R., l986. Cliff swallow colonies as information centers. Science 234:83-85.
- Brown, C. R. and M. B. Brown, 1986. Ectoparasitism as a cost of coloniality
in cliff swallows (Hirundo pyrrhonota).
- Brown, C. R., 1984. Laying eggs in a neighbor's nest: benefit and cost
of colonial nesting in swallows. Science 224:
Senior Scientific Staff:
- Mary Bomberger Brown, Research Associate (M.S., 1982, University of Nebraska-Lincoln)
- Amy Trachte, Research Associate (B.S., 2004, University of Oklahoma).
Research Students and Products (Current):
- Bridget Stutchbury (Ph.D., 1990,Yale): Plumage color and reproductive
tactics in male purple martins.
- Bruce Rannala (Ph.D., 1995, Yale): Demography and population structure
in island populations
- Jeffrey Davis (M. S., 1998): Costs and benefits of coloniality in purple
- Sarah Huhta (M. S., 1999): Reproductive success and coloniality in bank
- Christine Sas (M. S., 2000): Ecological correlates of colony size in cliff
- Cheryl Ormston (M. S., 2001): Breeding-site characteristics and range
changes of culvert-nesting swallows in Texas.
- Ana Briceno (M.S., 2002): Tail length and sexual selection in the North American barn swallow.
- Heath Weaver (M. S., 2002): The costs and benefits of coloniality in cave swallows.
- Thirty-three undergraduate student research projects since 1985.
- Sixty-five undergraduate research assistants since 1982
- Editor in chief, Journal
of Field Ornithology
- Associate editor, Behavioral
Ecology and Sociobiology
- Chair, Undergraduate Committee
- Member, Graduate Committee