(BOOK) Behavioral Ecology of Tropical Birds PDF

Preface
The idea for this book arose out of necessity. We needed information on
mating systems in tropical birds to compare with D N A fingerprinting
studies of temperate birds. We were asking a simple question: is extra-
pair mating more common in temperate than in tropical passerine
birds? We found little information on tropical birds. So we started some
empirical field studies in Panama to answer our own question, and
found no extra-pair fertilizations in the Dusky Antbird. But we
expected to find EPFs in the Clay-colored Robin because we knew
from our prior research that they bred synchronously during the dry
season, much like temperate zone birds do in the spring. A reviewer of
our paper stated that the prediction that Clay-colored Robins should
have EPFs qualified us for membership in the Flat Earth Society.
Extra-pair mating systems in passerines were (and still are) considered
ubiquitous, so it seemed silly to the reviewer that we were making a big
issue of predicting that robins would have EPFs. We had come face to
face with the Temperate Zone Bias.
Of course this was not the first time. E S M began working in Panama
in the 1960s, before behavioral ecology blew on the embers of the dying
field of ethology. Early work included latitudinal differences in avian
frugivory and fruiting seasons, the influence of nest predation on
breeding seasons, and the bioacoustic basis for the evolution of songs
in tropical birds. Major differences between temperate and tropical
birds were highlighted.We then turned to migratory birds.What a great
opportunity they provide to contrast adaptations to differences in
latitude within the same individual. But through all these endeavors, it
remained our impression that studies of temperate zone birds provided
the data to model generalities, and that tropical exceptions were con-
sidered oddities. Today, the now vibrant field of behavioral-ecology is
still much too reliant on_Lhese temperate-based models.
There is an intellectual vacuum to fill. We planned this book, not to
fill the vacuum, an impossible task, but to stimulate others to work on
tropical birds using a new perspective. The new perspective is exciting.
viii BEHAVIORAL ECOLOGY OF TROPICAL BIRDS
Our premise is not 'why tropical birds are so different' but rather 'why
temperate zone birds are so atypical.' Alexander Skutch (1985) used
the same logic when he stated that the question should not be 'why do
tropical birds lay so few eggs?' but, rather, 'why do temperate zone birds
lay so many?'The answer seems more tractable when you ask it in this
way.
In the tropics diversity is the name of the game. For example, over
90% of North American passerines have a similar territorial system,
they defend breeding territories for only a few months each summer.
But, in the tropics, only 13 % of passerines defend territories during the
breeding season only; instead the predominant territorial system is
year-round defense of feeding and nesting territories plus three other
systems not represented at all in temperate zone passerines! Our
message is clear. In order to discover generalities about avian biology, a
diversity of adaptations helps provide the comparative material needed
to overcome the thin slice of time represented by the present. And,
while understandable, a temperate zone bias is inexcusable, because it
is more than a latitudinal bias, it acts as a blinder to the amazing diver-
sity in behavioral adaptations that remain to be explained.
We also have regrets. We apologize for the heavy load we place upon
passerine birds in this book. We hope that the ideas are generalizable to
other groups. Passerines make good subjects, though, because they are
mainly freed from stringent nest site requirements and there are so
many species. Our focus on the neotropics is due to our familiarity with
the natural history of the birds there.
This familiarity is due largely to the efforts of two mentors, Martin
Moynihan and Eugene Eisenmann. Both were instrumental in the
development of tropical bird study and in the development of one of
the premier tropical research institutions, the Smithsonian Tropical
Research Institute (STRI). STRI afforded E S M both predoctoral and
postdoctoral opportunities to become familiar with tropical birds and,
for both of us, a yearly visit to Panama for research.We thank STRI staff
for their help in facilitating our field research, and their excellent library
was an invaluable resource for us.
Readers will see, time and again, that we draw conclusions and make
generalizations based on evidence from just a few studies and species.
For most important questions there are not enough data to perform
formal comparative analyses of temperate versus tropical species.
Instead we take the few pieces of the puzzle that exist, and our own
experience, and try to see the big picture. We cannot wait until dozens
of studies have been done on a variety of tropical birds to tackle
PREFACE ix
particular questions. The slow but steady rate at which such studies are
being done means that the tropical ecosystem will be largely ruined by
the time such comparative studies could be made. But important dif-
ferences in ecology and behavior do exist, and it is very clear that
temperate species are not a good model for understanding the behav-
ioral ecology of tropical birds.
This book is a call to arms. We highlight the missing pieces of the
puzzle in the hope that an army of graduate students and researchers
will set out to find the answers before it is too late. Our fervent wish is
that residents in tropical countries will be stimulated to answer the
many questions we raise. Opportunities abound for discovering,
describing, and discussing the beautiful ways tropical birds are differ-
ent from run-of-the-mill temperate zone birds and yet more
representative of avian adaptations worldwide.
We thank Isabelle Bisson, Debbie Buehler, Sharon Gill, Gail Fraser,
Joan Howlett, Jennifer Nesbitt, Ryan Norris, and Trevor Pitcher for
reviewing and commenting on various chapters in this book. The
Smithsonian Institution, through its Scholarly Studies Program, and
the Natural Sciences and Engineering Research Council of Canada
provided essential grant monies to carry out our research and support
students. York University provided excellent support for field research
by BJMS and her students, and much of this book was written during
her sabbatical leave. Stan and Pat Randprovided us with a place to stay
and a trusty Cherokee to ride in for several years.We are forever grateful
to them. We also thank Douglas and Sarah who were born to the task.
Bridget J. M. Stutchbury
Eugene S. Morton
Why are tropical birds
1
interesting?
1.1 Ecology and breeding seasons

'Tropical birds' brings to mind exotic and showy species like motmots,
toucans, parrots, manakins, birds of paradise and groups like the antbirds
which are restricted entirely to the neotropics. One pictures a lush humid
jungle where these birds thrive year-round, though tropical habitats
include savannahs, mangrove and dry forests. The sheer number of dif-
ferent species is overwhelming. It is a simple matter to show a first-time
visitor, as we have done in Panama, more than 75 new species of birds in
their first morning. A small country like Panama has some 900 species of
birds (Ridgely and Gwynne 1989), more than all of North America! Even
more impressive because Panama comprises an area (about 75,000 km 2)
equivalent to the state of South Carolina. This amazing species diversity
is well known to most biologists and naturalists.
Not fully appreciated is the fundamentally different ecology that
tropical birds exhibit. Daylength and temperature do not vary season-
ally to any great extent. There is no such thing as winter, with short
daylight coupled with bitterly cold temperatures. The year is divided
into the dry season and wet season not the spring, summer, winter, and
fall seasons of the temperate zone.The timing and length of the dry and
wet seasons varies with locale and latitude (Figure 1.1). The wet season
north of the equator often occurs from May through November, and
below the equator at the opposite time of year. Near the equator there
are often two dry and wet seasons each year. In some areas there is no
distinct dry season (see Forsyth and Miyata 1984, Kricher 1997 for
overview). In other areas a prolonged dry season results in a deciduous
forest, where some or all trees drop their leaves to reduce water loss.
Food is still abundant, however, as nectar and fruit are produced in
large supply (Morton 1973, Janzen 1975, Foster 1982, Fleming et al.
1987). The year-round availability of food means that most species are
residents (non-migratory) and many that eat insects defend territories
all year. Intra-tropical and altitudinal migration occur, but are
restricted mostly to frugivores (Morton 1977, Levey and Stiles 1992).
BEHAVIORAL ECOLOGY OF TROPICAL BIRDS
Figure 1.1
Timing of the wet season (shaded) in east Africa at different latitudes and times
of year (after Moreau 1950).
Unlike birds of the temperate zone tropical birds breed at all times of
the year. Frugivorous birds often breed during the dry season, whereas
insectivorous birds breed during the longer wet season (Morton
1971 b, Morton 1973). Breeding seasons, typically four to eight months
long (Ricklefs 1969b, Kunkel 1974), are timed to coincide with fruit or
insect abundance or reduced predation pressure, not climate per se
(Chapter 2). This contrasts sharply with the temperate zone where
climate is a major constraint that forces birds to breed quickly, within
two to three months.
Tropical/temperate zone differences in migratory behavior and
breeding season set the stage for major differences in social behavior.
This book describes and evaluates the evolutionary consequences of
these latitudinal differences as they affect life history traits, mating
systems, territoriality and communication. The first simple and broad
generalization has already been alluded to: species in temperate regions
are under strong selection from abiotic factors (e.g. climate) whereas
in tropical regions biotic selection pressures are most important.
WHY ARE TROPICAL BIRDS INTERESTING?
Interactions with other species (plant and animal) play a key role in
shaping the behavioral adaptations of tropical birds, and are the subject
of the final chapter.
1.2 Speciesdiversity
Most biologists identify taxonomic diversity as the greatest difference
between temperate zone and tropical birds. Species diversity increases
dramatically in the tropics. For instance, there are only 5 genera of
tyrant flycatchers in eastern Canada and the U.S., but a remarkable 79
genera in tropical Brazil (Figure 1.2). Similarly for hummingbirds and
tanagers (1 versus over 30 genera). Other families like hawks and wrens
show a similar but less dramatic pattern (Figure 1.2). Many of our tem-
perate zone birds derive from tropical ancestors. Some groups, such as
antbirds, do not occur at all in north temperate areas.
Much tropical research has focused on documenting and under-
standing patterns of diversity throughout the tropics (Remsen 1984,
Terborgh et al. 1990, Thiollay 1994), often as part of a strategic biodi-
versity assessment program. These research efforts have led to the
Figure 1.2
Number of genera within each family at different locations in the New World
(eastern Canada, southeastern US, Mexico, Panama, and Brazil). Families are
Accipitridae (hawks, eagles, kites), Troglodytidae (wrens), Tyrannidae (flycatch-
ers) and Formicariidae (antbirds). The dashed lines indicate the latitudinal
boundaries of the tropics (23~ and 23~ Drawings from Sick (1993), Owings
and Morton (1998), Skutch (1997) and Wetmore (1972).
discovery of new species (e.g. Robbins et al. 1994, Kennedy et al. 1997,
Whitney and Alvarez 1998). Part of the mystique of the tropics is the
continual discovery of new species, something that rarely (if ever)
happens in north temperate regions. Without a doubt, an emphasis on
species diversity helps identify areas important for conservation.
We are all too familiar with the shocking facts. Tropical forests are
being cut at a rate of some 100,000 ha y-1 in the Philippines, 1.5 million
ha y-1 in Brazil, etc. Worldwide this adds up to 15 million ha y-~. For
most people, though, these statistics are too impersonal to really hit
home. Anyone who has visited tropical regions can see for themselves,
endless miles of landscape of scrubby and often eroded grass where
lush tropical forest once stood. Favorite study sites or birding spots that
when revisited a few years, or even months or weeks later, are barren of
trees. Tropical habitats are being destroyed so quickly that without
basic information on which species occur where, and in what numbers,
we cannot develop a strategy for saving biodiversity.
But another kind of diversity has been largely neglected in the rush
to catalog the occurrence of bird species. Biotic interactions have
shaped a behavioral and morphological diversity in tropical birds that
is far richer than that found in temperate zone birds. Understanding
the behavioral diversity of tropical birds requires that the selection
pressures underlying the traits can be inferred from current processes.
With the alarming loss of tropical habitats we lose not just the individ-
uals of a given species, but also the ability to study and understand the
remarkable adaptations represented through these species. History is
being lost. The strong biotic selection pressures mean that disruption of
the environment and loss of species can quickly erase the evidence nec-
essary to piece together evolutionary processes in the tropics.
Ant-following birds are among the first to disappear from forest frag-
ments, along with members of mixed species flocks (Chapter 7).
1.3 Temperate zone bias in behavioral ecology

It is ironic that tropical birds are viewed as strange, and perhaps even
bizarre, when they vastly outnumber temperate zone species (Figure
1.2). About 80% of all passerine species breed in tropical regions.
Likewise for other bird groups many of which do not occur outside of
the tropics. Temperate zone birds form a minority species group that
have converged to adapt to a temperate climate. Because of their world-
wide dominance, tropical birds typify the adaptive realm of birds and it
is their natural history that should be viewed as the n o r m for birds.
Shockingly little is known about most tropical birds, even their basic
natural history.
Most theory in avian behavioral ecology comes from models and
empirical studies of birds in temperate regions.We contend these theories
do not apply equally well to tropical birds, because the ecological and
social backdrop for tropical birds is fundamentally different. There is a
temperate zone bias because the vast majority of biologists are based in
temperate regions of North America and Europe, many of whom are
ignorant of the unique ecology and behavior of tropical birds. Often these
behavioral ecologists and ornithologists do not realize that the conven-
tional wisdom applies only to a select group of birds from temperate
regions, birds that do not represent general adaptations of birds.
Several temperate zone species stand out as frequently used models
for testing behavioral ecology theory. More behavioral ecology papers
have been published on the Red-winged Blackbird, Agelaius pheoniceus,
(Searcy and Yasukawa 1995, Beletsky 1996) than for all tropical birds
combined. One could just as easily substitute the Barn Swallow,
Hirundo rustica (Moiler 1994) or Great Tit, Parus major. This is not a
criticism of these studies, but a way to put the temperate zone bias in
perspective. Yet why shouldn't the Dusky Antbird or some other
tropical bird be our model of a typical bird?
Behavioral ecology has not ignored tropical birds or tropical adapta-
tions. The tropics, however, is generally viewed as a place to go to study
oddities, or in other words, phenomena that are u n c o m m o n in the tem-
perate zone. Many researchers have focused their attention on
cooperative breeders (Emlen 1981, Ligon 1981, Rabenold 1990,
Komdeur et al. 1995, Restrepo and Mondrag6n 1998) and lekking
species (Foster 1981, Trail 1985, McDonald 1989, Westcott 1997),
even though these types of social organization do not predominate in
the tropics (Kunkel 1974). Other tropical phenomena, like ant-follow-
ing (Willis 1967, 1972, 1973, Willis and Oniki 1978), mixed-species
flocks (Moynihan 1962, M u n n and Terborgh 1979, Powell 1985), and
duetting behavior (Farabaugh 1982) have similarly been well studied.
Tropical specialties attract attention precisely because they are
clearly different from temperate zone systems. The more typical
tropical birds are socially monogamous, wherein a male and female
defend a territory and raise young together, and defend territories year
round (Chapter 5). They may appear the same as their temperate zone
counterparts, but recent research has shown that they differ in many
ways. The division of labor between members of long-term monoga-
mous associations is nearly equal but has been described for only a few
tropical species (e.g. Greenberg and Gradwohl 1983). These typical

tropical species have an impressive number of complex and unique
adaptations which are only beginning to be described and appreciated.
Below we give an overview of several examples where extensive
research on temperate zone species has led to broad generalizations
about birds, but where tropical birds differ dramatically from these
temperate zone systems. This is an overview of more detailed treatment
in later chapters.
1.4 Examples of temperate zone bias

Extra-pair mating systems
Over the past decade, genetic testing of parentage (usually via D N A
fingerprinting) has spawned many studies revealing that extra-pair fer-
tilizations (EPFs) are common in species previously considered to be
monogamous. A female has a single social mate with which she raises
young, but a proportion of her young (often over 20%) are derived
from copulations with males other than her social mate (Birldaead
and Moiler 1992). Hence the current distinction between social
monogamy (raising young together) versus genetic monogamy (mating
exclusively with each other). Although there is much variation in E P F
frequency among species (Stutchbury and Morton 1995,Westneat and
Sherman 1997), the majority of socially monogamous passerines
studied to date have an extra-pair mating system. EPFs drive the evo-
lution of anti-cuckoldry behaviors in males and underlie sex role
divergence in reproduction. Extra-pair mating systems are now consid-
ered the norm for most birds. Consider the following quote from
Birkhead and Moiler (1996, p.323) 'Until recently monogamy was also
assumed to imply an exclusive mating relationship between two indi-
viduals (Wittenberger and Tilson 1980), but recent behavioral and
molecular studies (reviewed in Birkhead and Moiler 1992) have shat-
tered the illusion of sexual fidelity: in the majority of species extra-pair
copulations and fertilizations outside the pair bond occur routinely'.
But are extra-pair mating systems the norm? The majority of parent-
age studies on socially monogamous birds (over 90%) focus on
temperate zone breeders. Male tropical passerines have smaller testes
than temperate zone species, often 1/10th the size, which predicts a low
level of sperm competition among these males and few EPFs in tropical
species (Stutchbury and M o r t o n 1995). The handful of socially
monogamous tropical birds fingerprinted have few (< 15%) or no
extra-pair young (Chapter 4). Extra-pair matings are likely to be
relatively u n c o m m o n in socially monogamous tropical birds and,

therefore, extra-pair mating systems are not the norm for birds.
This dramatic difference in mating system stems from differences in
the length of breeding season which are determined largely by latitude
and which cause differences in breeding synchrony between the tem-
perate zone and tropics. Across passerine species, as nesting synchrony
increases so does the percentage of broods that contain young derived
from EPFs (Chapter 4). The tropics show us that extra-pair mating
systems are not typical of passerines, as thought by most biologists.
Instead, climatic conditions force temperate zone birds to breed syn-
chronously, and synchronous breeding, in turn, fosters the evolution of
extra-pair mating systems (Stutchbury and Morton 1995, Stutchbury
1998a).
Testosterone and territory defense

A high level of testosterone in male birds is thought to be critical for
successful territory defense and increasing male attractiveness to
females. For example, in socially monogamous species, levels of testos-
terone are high early in the breeding season during territory
establishment and pair formation, but drop when males are feeding
young (Wingfield and Moore 1987, Wingfield et al. 1990). Male testis
size increases dramatically prior to breeding. In polygynous species,
where male parental care is lower and mate attraction persists for most
of the season, testosterone levels remain high (Beletsky et al. 1995).
When testosterone levels in males are experimentally increased, male
parental behavior is suppressed but male attractiveness to females
increases (Wingfield 1984, Oring et al. 1989, Ketterson et al. 1992),
including success in getting extra-pair fertilizations (Raouf et al. 1997).
Recent studies show that this scenario does not fit tropical birds
(Chapter 5). Males of tropical species retain small testes even during
the breeding season, and have low levels of circulating testosterone
despite having vigorous territory defense and song output. This shows
that high testosterone level is not a prerequisite for successful territory
defense and mate attraction. Instead, high testosterone in temperate
zone birds should be viewed as an adaptation to compete successfully
for mates and extra-pair matings during the short temperate breeding
season.Thus constrained to nest synchronously, temperate birds evolve
specific adaptations to compete within the extra-pair mating systems
there, one of which is a crucial reliance on hormonal 'jacking up' based
on testosterone.
Territory acquisition
Territory establishment by the male, followed by mate attraction, is the
common model of territory defense (Freed 1987). In this kind of territo-
rial system, dominated by long-distance migrants of the temperate zone,
males and females have many unoccupied areas for establishing territo-
ries when they return in spring. Territory defense against males intruding
for extra-pair matings is crucial for males (Stutchbury 1998b). Song,
primarily a male trait, coincides with territory establishment, mate
attraction and EPF competition. Tropical birds, many of which are year-
round residents, face dramatically different opportunities and constraints
in acquiring a territory and mate. Year-round territoriality, stable terri-
tory boundaries and high adult survivorship results in a low turnover rate
on territories (Chapter 5). Extra-pair matings are uncommon, so
boundary disputes by males and females are about real estate. Territorial
openings occur relatively infrequently so males and females alike have
few opportunities to choose mates. Singing occurs at a relatively low rate,
often by both sexes, and functions primarily in territory defense rather
than mate attraction or EPF competition (Chapter 6).
Although opportunities to switch territories are scarce, individuals
are primed to do so. This can be demonstrated by capturing and detain-
ing territory owners for several days to create vacancies experimentally.
Our own work on the Dusky Antbird, Cercomacra tyrannina, shows that
males and females quickly (usually within hours!) abandon mates and
territories when given the chance (Morton 1996b, Morton et al. 2000).
Within minutes of 'losing' their mate, both sexes begin singing a
courtship song to attract a new mate. This, despite the fact that Dusky
Antbirds often remain with the same mate for five or more years,
defend year-round territories, and sing in duets. Similar results have
been found for several other tropical passerines where temporary
removals have been conducted (Levin 1996a, Gill and Stutchbury, in
prep.).
We will expand on the examples above, and others, to convince nat-
uralists and behavioral ecologists that lessons learned from the
temperate zone do not necessarily apply in tropical regions. The main
theme of this book is to illustrate where, how and why tropical birds are
so different from temperate zone birds. The book's purpose is to dispel
the temperate zone biologists' ignorance of tropical biology and to
stimulate more research on tropical birds. To this end we suggest a the-
oretical framework based upon latitudinal differences in extra-pair
mating and biotic interactions and their influence on life history traits
in tropical birds.
2 Breeding seasons
Interest in what controls the timing of breeding in birds goes back to

earlier ornithological studies (Moreau 1937, Nice 1937, Baker 1938),
many decades before behavioral ecology was known as a distinct field.
In spite of the numerous early studies of breeding seasons, many of
which focused on tropical birds (e.g. Skutch 1950, Miller 1962,
Ricklefs 1966, Fogden 1972, Sinclair 1978), the question of how selec-
tion affects timing of breeding remains a popular and important
question in behavioral ecology (Martin 1987, Svensson and Nilsson
1995, Schoech 1996, Svensson 1997). The first, and still most widely
accepted, hypothesis is that the availability of food determines when
birds breed (Lack 1954, Perrins 1970). The tropics are an especially
good place to test this idea because of the great variability among
species in diet and their timing of breeding.
2.1 Seasonality in tropical breeding seasons

The tropics are often viewed as rather benign with respect to climate,
and since food is generally available year-round, one might expect
tropical birds to breed year-round. While it is true that in some species
and areas breeding can occur throughout the year (e.g. Miller 1962,
Tallman and Tallman 1997), most tropical birds show surprisingly
strong seasonality in breeding (Skutch 1950, Sinclair 1978, Boag and
Grant 1984). There are distinct and more or less predictable times of
the year when a species does not breed. Two general patterns distin-
guish tropical breeding seasons from temperate zone ones: (1) greater
length of breeding season in the tropics, and (2) greater variability
among species (and individuals) in when breeding occurs.
Tropical species are characterized by breeding seasons that are two
to three times as long as those typical for the temperate zone, and this
applies to a variety of bird groups worldwide (Baker 1938, Skutch
1950, Ricklefs 1966, Wyndham 1986). For example, averaging
breeding season length for a large number of species (mostly passer-
ines), Ricklefs (1966) found breeding season length to range from 3.1
10 BEHAVIORAL ECOLOGY OF TROPICAL BIRDS
Figure 2.1
Breeding season length for A) Typical temperate zone passerine, the Hooded
Warbler, Wilsonia citrina (Evans Ogden and Stutchbury 1996) B) Rufous-collared
Sparrow, Zonotrichia capensis (Miller 1962), C) Mangrove Swallow, Tachycineta
albilinea (Moore et al. 1999) and D) White-fronted Bee-eater, Merops bullokoides
(Wrege and Emlen 1991). Drawings from Owings and Morton (1998), Wetmore
(1984), and Krebs and Davies (1991).
BREEDING SEASONS 11
to 4.2 months in the temperate zone, and 6.6 t o 9.8 months in tropical
regions. In a broad review, Baker (1938) found a similar latitudinal
pattern in breeding season for avian groups such as seabirds, herons,
ducks and raptors.
North temperate species of landbirds generally breed at the same
time, May-July (Figure 2.1). Short breeding seasons in temperate zone
species clearly result from climatic constraints; there is only a short
window of opportunity where temperatures and food supply allow suc-
cessful breeding. In temperate regions, there is little variation among
species and individuals in when breeding occurs. Most passerines
breed in the spring and early summer, and species differ by only a
matter of weeks in when breeding is initiated (Lack 1950). Within
species, most individuals lay their first clutch within a few weeks of each
other. Detailed studies on Blue Tits, Parus caeruleus, and Great Tits,
Parus major, examine the adaptive significance of differences of only
several weeks in clutch initiations (Perrins 1991, Nager and van
Noordwijk 1995, Ramsay and Houston 1997).
Their tropical congeners have much longer breeding seasons, which
vary in time of year from species to species (Figure 2.1). Breeding
seasons of different species and individuals are often separated by
months rather than weeks. All kinds of patterns can be found in the
tropics. Some species breed primarily during the dry season months
and others during the wet season. As the timing and length of the dry
season changes with latitude, so do the breeding seasons (Snow
1976a). Seasonality is often more pronounced at high altitudes where
breeding seasons are shorter (Skutch 1950). In some areas where there
are two wet seasons, species show two peaks of breeding activity during
the year (Miller 1962,Wilkinson 1983). The breeding seasons of indi-
viduals within a species may vary greatly (e.g. Robinson et al. 2000)
raising the question of why some individuals begin breeding months
before others.
Extreme differences in breeding season can also occur over very
short distances (Wrege and Emlen 1991). In montane areas of western
Cameroon, lowland populations breed 5-6 months later than con-
specifics in higher altitude populations only tens of kilometers away
(Tye 1991). Clay-colored Robin, Turdus grayi, populations in Panama
separated by only 30 km breed several months apart (Morton 1973;
Figure 2.4). The question, then, is: can food availability predict the
timing of breeding in tropical birds?
2.2 Food availability and timing of breeding

The food availability hypothesis suggests, in its simplest form, that
birds should breed when food is abundant for raising young (Lack
1954). This should be especially important for birds with altricial
young that require extensive provisioning by parents. Perrins (1970)
argued that food for producing eggs may constrain timing of breeding
because females that lay too early can pay a high price if food abun-
dance is low. In the temperate zone food abundance changes drastically
in spring over a few weeks, so there is likely a tradeoffbetween produc-
ing eggs at the best time versus hatching young at the best time.
The food availability hypothesis has been generally supported in the
temperate zone. In particular, detailed studies on European tits have
shown that egg-laying is timed so that the nestling period coincides
with a 2-3 week period of caterpillar abundance in spring. Individuals
that lay early or late (naturally, or due to experimental manipulations)
suffer increased nestling mortality (Perrins 1991, van Noordwijk et al.
1995). Blue Tits supplemented with food advance egg-laying signifi-
cantly, but by less than a week (Nilsson and Svensson 1993). Mainland
and Mediterranean Blue Tits at a similar latitude differ by three weeks
in the onset of laying in response to consistent differences in the avail-
ability of caterpillars (Zandt et al. 1990). This adaptive behavior has a
genetic basis and results mainly from differences in responsiveness to
similar daylengths (Lambrechts et al. 1996). These kinds of details, or
anything close to it, are not available for any tropical species.
A simple prediction of the food availability hypothesis is that diet
should explain the breeding seasons of different tropical species. Fru-
givorous species should breed when fruit is abundant, nectarivorous
species when flowers are abundant, and insectivorous species when
arthropods are most abundant. Examples where breeding seasons gen-
erally correlate with rainfall or food abundance are numerous. In
Central America, Skutch (1950) reported that nectarivorous birds
(hummingbirds) breed during the dry season (January-March), which
is when flowers are most abundant. In contrast, birds that eat grass
seeds (e.g. Sporophila) breed only later in the year (June-August), well
after the wet season begins and enough time has passed for the grass to
form new leafy shoots, flower and begin to set seed. In a tropical
African savannah, the peak in nesting activity of insectivorous birds
occurs from December through June, which is when rainfall and insect
abundance is high (Sinclair 1978). Little or no reproduction occurs
during the dry season months (July-October). These sorts of broad
BREEDING SEASONS 13
comparisons, which lump many species together into ecological

groups, provide only a weak correlation between breeding seasons and
food supply at the individual level. Formal comparative studies, which
take phylogeny into account, have yet to be done.
A more convincing test would be to show that peaks in breeding
activity within a given species coincide with peaks in food abundance.
Relatively few studies have actually measured food abundance and cor-
related this with clutch initiations, and these have provided mixed
results. Opportunistic breeding in Darwin's Finches, Geospiza, begin-
ning soon after major rainfall, has been interpreted as support for the
food availability hypothesis (Boag and Grant 1984). But this does not
explain why some individuals begin breeding before the rainfall, and
long after food abundance has declined (Boag and Grant 1984). In a
hummingbird, the Long-tailed Hermit, Phaethornis superciliosis, there is
a bimodal pattern of nesting activity which corresponds roughly to the
two annual peaks in flower availability (Figure 2.2; Stiles 1980).
Nectarivorous Hawaiian honeycreepers, the Apapane, Himatione
sanguinea, and Iiwi, Vestaria coccinea, also have peak breeding activity
when flower abundance peaks (Ralph and Fancy 1994). In the White-
crowned Pigeon, Columbia leucocephala, nesting was closely related to
the abundance of one particular fruiting plant (Bancroft et al. 2000).
But there are also many examples where food peaks do not coincide
closely with breeding. In two species of manakins (Pipra mentalis and
Manacus candei), both of which are almost entirely frugivorous,
breeding peaked when fruit abundance was lowest (Figure 2.2; Levey
1988). In several insectivorous species, breeding peaks before arthro-
pod abundance peaks (Figure 2.2; Gradwohl and Greenberg 1982,
Young 1994, Komdeur 1996). Similarly, peaks in breeding often
precede peaks in rainfall (and presumably food abundance) by several
months in other insectivorous birds (Wunderle 1982,Wilkinson 1983,
Woodall 1994). It is paradoxical that the peak period for breeding
occurs several months before food availability peaks, and such findings
certainly seem inconsistent with the food availability hypothesis.
A resolution to this apparent contradiction may come, in part, with a
more precise definition of how food availability affects individual
fitness. Frugivorous and nectarivorous species likely depend on high-
protein insect food for feeding their young (Morton 1973), so this may
explain why in some species, like the manakins, breeding occurs when
insects, rather than fruit, are at the peak abundance (Levey 1988). But
why should insectivorous species breed when arthropod abundance is
low? In tropical species where clutch size is low (Chapter 3) and
Figure 2.2
Timing of breeding and food abundance for A) Long-tailed Hermit, Phaethornis
superciliosus (Stiles 1980; % nests started and number of foodplants in full
bloom), B) White-collared Manakin, Manacus candei (Levey 1988; % individuals
captured in breeding condition and total number plants with ripe fruit) and C)
Tropical House Wren, Troglodytes aedon (Young 1994; % clutch initiations and
arthropod biomass). Drawings from Blake (1953).
BREEDING SEASONS 15
breeding vacancies scarce (see Chapter 5), reproductive success may be

limited by the survival and successful dispersal of fledglings, rather than
by the ability of parents to feed a large brood of nestlings in the nest.
Fledglings often remain on their parent's territory for many months
after they leave the nest, and this period may be crucial for their survival.
In Tropical House Wrens, Troglodytes aedon, arthropod abundance was
highest at the time of juvenile dispersal and molt (Young 1994) suggest-
ing that juvenile survival may be dependent on abundant food.
To understand the selective forces at work, one needs to study the
consequences of early versus late breeding on the reproductive success
of individuals within a population. In other words, to assess the fitness
consequences of different reproductive tactics. Although this approach
is common in temperate zone studies (Perrins 1991, van Noordwijk et
al. 1995), few studies on tropical species have attempted to measure the
costs and benefits of breeding at different times. Do individuals that
nest very early, or very late, suffer in terms of offspring production? Do
the fledgling house wrens produced by early nesting pairs in February
(Figure 2.2) have a lower survival or dispersal success because insect
abundance is still low when they fledge? Reproductive success in Sey-
chelles Warblers, Acrocephalus sechellensis, is highest for nests begun two
months prior to the peak in food abundance (Figure 2.3; Komdeur
1996). Two months is the period required for nest construction, laying
0 - - 160
==60- -120 oo
,C
0
>- "0
E 40
(9 e~
"r0 <
~20
(9
-40 ~
"0 c
_=
0 -0
-7 -6 -5 -4 -3 -2 -1 0 1 2 3 4
Month Relative to Food Peak
Figure 2.3
Figure 2.3. Percentage of Seychelles Warbler, Acrocephalus secheilensis, clutches
producing independent young in nests begun at different times of the year (open
bars) relative to the peak insect abundance (solid line) which usually occurs some
time from July-September. Data from Komdeur (1996).
and incubation, so most pairs have nestlings at the time of peak food
abundance.
Experimental manipulations of food supply are one way to deter-
mine how selection is operating on individuals. This approach has been
used extensively for temperate zone species, where dozens of studies
have shown that food supplementation affects timing of breeding by
advancing egg-laying dates (reviewed in Martin 1987, Svensson and
Nilsson 1995, Schoech 1996). Such experiments have rarely been con-
ducted on tropical species; in fact, we know of only one example. In an
African eagle, Aquila wahlbergi, food supplementation did not induce
earlier laying (Simmons 1993). Komdeur (1996) did manipulate food
supply in the Seychelles Warbler, not through food supplementation
but through translocation of breeding pairs to islands with differing
food supply. Pairs transferred to islands with higher food abundance
had prolonged breeding seasons and higher annual reproductive
success, compared with their own breeding histories prior to the
transfer. Given the very broad variation in timing of breeding among
individuals in some populations, food supplementation experiments
have the potential for dramatic effects.
2.3 Nest predation and molt

While the food availability hypothesis is strongly supported with
detailed experimental studies in the temperate zone, there is much con-
flicting evidence from studies on tropical birds. There are many
examples where tropical birds do not breed at a time when food for pro-
ducing eggs or feeding young is most abundant. These temperate zone
hypotheses (Lack 1954, Perrins 1970) explain breeding seasons that
are constrained by the temperate zone climate. Other factors must be
considered to explain tropical breeding seasons such as nest predation,
molt, and sexual selection.
Nest predation on tropical birds can be very high (80-90% of nests,
Chapter 3), and predation risk often varies seasonally. Morton (1971 b)
suggested that Clay-colored Robins breed at a time when food is scarce
in order to avoid seasonal peaks in nest predation. Avoidance of nest
predation may also explain why Bananaquits, Coerebaflaveola, begin
breeding long before the wet season begins (Wunderle 1982). Food is
likely scarce during the dry season as clutch sizes and nestling weights
in large broods are lower for nests begun before the wet season.
However, nest predation on Bananaquits increases from 30% in the
dry season to 72% in the wet season.
BREEDING SEASONS 17
Nest predation does not explain all examples of early breeding by

insectivorous species. In HouseWrens nest predation risk does not vary
seasonally (Young 1994). In Dot-winged Antwrens, Microrhopias quix-
ensis, predation risk was much higher on nests begun early in the wet
season (Gradwohl and Greenberg 1982). Since the only successful
nests were those begun late in the wet season, early breeding cannot be
explained as an escape from nest predation.
The timing of breeding may be determined by selection on the
timing of molt. Molt is energetically expensive, and there is much
evidence that tropical species avoid molt at times of year when food is
scarce (Fogden 1972, Poulin et al. 1992). Breeding and molt generally
overlap little or not at all for individuals within a breeding population
(Levey and Stiles 1994, Ralph and Fancy 1994, Tallman and Tallman
1997) or within the avian community as a whole (reviewed in Foster
1975). Most species have a distinct molt season that follows breeding,
and the molt is more regular in its timing than the breeding season (e.g.
Snow 1962, 1974, Fogden 1972, Levey and Stiles 1994). It has been
argued that this regularity in the timing of molt means that molt is
'fixed' in its timing which in turn constrains the timing of breeding
(Snow 1962, 1974).
Species where individuals extensively overlap breeding and molt
generally have a very protracted molt (6-9 months), which likely
reduces the costs of overlapping two energetically expensive activities
(Stiles and Wolf 1974, Wilkinson 1983, Levey and Stiles 1994). For
instance, in the Long-tailed Hermit individuals differ by as much as 6
months in the initiation of molt (Stiles and Wolf 1974). Some males
display on leks while in full molt, while others have no overlap between
displaying and molting. Remarkably, individuals molt at the same time
(+ 2 weeks) each year.
However, there is no direct evidence indicating that molt determines
breeding seasons. While molt could force birds to end breeding while
food is still abundant, it does not explain why breeding begins when it
does. As Levey and Stiles (1994) note, the effect of molt on breeding
seasons remains poorly understood and studies following marked indi-
viduals over several seasons are needed to determine the consequences
of different molt/breeding strategies. No studies have examined
whether individuals who overlap breeding and molt are at any selective
disadvantage.
18 B E H A V I O R A L ECOLOGY OF TROPICAL BIRDS
2.4 Sexual selection and the breeding season of the

Clay-colored Robin
We mentioned earlier that the food availability hypothesis may or may
not operate in the tropics. Here we take a deeper look at an example
where food does not control the breeding season. Instead, the breeding
season may be molded by sexual selection to a greater extent than by
natural selection. In Panama, the breeding season of a tropical
songbird, the Clay-colored Robin, has characteristics that are difficult
to explain by natural selection alone. The first is that robins begin to
breed at different times in places separated by very short distances
(Figure 2.4). The breeding season may begin a month earlier on the
Figure 2.4
Timing of the start of the breeding season of Clay-colored Robins, Turclus grayi, in
the canal area of Panama (Morton, unpubl, data). Differently shaded areas
indicate dry, mesic or wet regions. Nestlings born in Panama City, but translocated
to BCI (arrow) and hand-raised there bred at the same time as the nearest local
birds on the mainland.
BREEDING SEASONS 19
Pacific coast, near Panama City, than 20 km inland at Summit

Gardens. Overall, breeding begins in January on the Pacific coast and
spreads slowly to the Atlantic, where, while only 80 km away, breeding
might not begin until mid-April. Such differences in the timing of
breeding over short horizontal distances are unheard of in the temper-
ate zone.
What factors might underlie the timing of breeding in robins? One
idea we examined is that breeding seasons are controlled genetically
and each population's breeding differs owing to underlying genetic dif-
ferences. Another idea focuses on food availability, which varies with
the beginning of the dry season. The dry season begins earlier and lasts
longest on the Pacific than on the Atlantic coast, which accords with
the robin's timing of breeding.We did an experimental translocation to
test whether genetics or local environment determined timing of
breeding. We handraised baby robins (n = 25) taken from the Pacific
coast and placed them in large flight cages on Barro Colorado Island
(BCI) in Gatun Lake, about halfway between the two coasts (Figure
2.4). BCI is entirely forested and was without wild robins. The nearest
population of robins was found in the town of Frijoles, about 3.2 km
away over water and well out of earshot of our caged birds. The captives
were fed food ad libitum, so food availability was not a factor. For
several years (1970-1974) these birds initiated breeding at the same
time (first week of March) as the wild birds at Frijoles and about four
weeks later than the Pacific coast population from which they came.
The captive robin data rule out either food availability or genetic dif-
ferences to explain their breeding time. Using natural selection, we
suggested that, instead, predation might affect the breeding season
(Morton 197 l b). Predation risk jumps from 58% of nests destroyed
during the dry season to 85% during the wet season, so predation
replaces nestling food abundance as the primary determinant of the
breeding season. Food availability for nestlings is lowest during the
robins' breeding season and most nests suffer severe brood reduction
through starvation of nestlings (Chapter 3).
Clay-colored Robins often fledge at very low body mass, basically as
runts (see also Chapter 3). Unlike many passerines, they continue to
grow in size long after they are independent of their parents. One con-
sequence of this adaptation is that the flight feathers they have as
juveniles end up being too small for their growing body. All captive-
raised birds molted their wing and tail feathers, in addition to the body
feathers, during the postjuvenal molt. Most tropical birds do not molt
flight feathers in the postjuvenal molt. The replacement of tail and
flight feathers by young robins must be an adaptation to their starva-

tion dry season diet. The nestling robin is caught in the 'altricial
strategy'. It cannot eat fruit because fruit will not enable it to grow at
the maximum rate needed to escape nest predation during the time its
body heat is provided by the mother. It must have high protein food for
that. Nestling robins will not eat fruit until they begin to regulate their
own body temperature (Morton 1973). As a consequence, brood
reduction through starvation is common, even though nestlings are fed
fruit much more so than temperate zone Turdus (Dyrcz 1983).
Another peculiar feature of robin breeding seasons is that the dawn
chorus of males and nesting activity begins abruptly within a popula-
tion (Stutchbury et al. 1998). Even within a population, there are areas
where individuals are highly synchronized with each other. In our study
site at Gamboa, Panama, for 3 years in a row 5 adjacent males along
one street began singing before any others, and the last group of males
began singing about 3 weeks later. Small cadres of males, perhaps they
could be termed leks (Wagner 1993), begin to sing nearly simultane-
ously, producing even higher synchrony than found in the town as a
whole.
So, even if we are satisfied that predator pressure pushes robins into
breeding when food for nestlings is lowest, we still cannot explain another
characteristic, their high breeding synchrony within any o n e location
(Stutchbury et al. 1998). None of the potential causes from natural selec-
tion can explain both breeding at the worst time for raising young and the
high localized synchrony in breeding in this tropical thrush.
Sexual selection provides an explanation for both. Females control
who mates with them. Females are larger than males in this robin
(Morton 1983). In robins, it is likely that male song output in the dawn
chorus, after males have been fasting during the night, might be the
currency females use in choosing males (Stutchbury et al. 1998). By
breeding synchronously, females choose males after assessing them
under the same ecological conditions (see Chapter 4). In other words,
breeding synchrony produces an even playing field upon which males
compete. Female choice, we suggest, produced the synchronous onset
of singing and nesting. One advantage to breeding in the dry season is
that males can recuperate from their singing marathons because food
for them is in greatest abundance. This food is fruit, especially Miconia
argentea, Xylopia sp., Bersera simaruba, and Panax morototoni in our
study area, all of which are abundant only in the dry season.
Breeding when ecological conditions favor male song output may
evolve if males that sing more mate more. In omnivores like robins,
BREEDING SEASONS 21
breeding seasons may not be the best time for feeding nestlings but the
best time for quickly eating fruit and then returning to singing. In this
way, sexual selection can influence the timing of breeding seasons.
Other species with strong sexual selection, particularly those with clas-
sical leks (manakins, cotingas) may also have breeding seasons that
cannot be explained entirely by natural selection. Once again, tropical
birds show that the temperate zone data stating that birds breed when
it is best for raising young, is not necessarily the case.
Although food availability for making eggs and feeding nestlings is
paramount for temperate species, this does not appear to be generally
true for tropical birds in terms of their breeding seasons. Food avail-
ability fine-tunes breeding seasons in some species, but in others
predation or sexual selection is more important.
2.5 P r o x i m a t e cues
Despite the long history of studies on tropical breeding seasons, little is
known about the proximate cues that stimulate individuals to become
physiologically prepared to breed. The proximate mechanisms that
have evolved can give Us insight into the ultimate factors that favor
breeding at a particular time. The great variability in breeding seasons
among species and individuals in the same locale, and from year to
year, suggests that short-term cues (rainfall, food availability, etc.)
must trigger gonadal growth.
While photoperiod clearly is the main cue used by temperate zone
birds, this cue has long been assumed as unimportant for tropical birds
because daylength varies so little near the equator. Ironically, this is an
instance where tropical birds are not so different. A recent study on a
neotropical forest passerine, the Spotted Antbird, H y l o p h y l a x nae-
vioides, showed that individuals can perceive the small one hour
differences in daylength that occur over the year in its natural habitat
(Hau et al. 1998). Individuals even responded physiologically to a pho-
toperiod increase of only 17 minutes. In the wild, gonadal growth
began 1-2 months prior to the wet season, presumably in response to
photoperiod, but short-term cues (rainfall, food) are responsible for
the fine-tuning of the start of breeding (Wikelski et al. 2000). If rainfall
is a cue, then we learn only that birds respond to indicators of the wet
and dry seasons and this does not address, at the ultimate level,
whether food availability, predation or other factors are important.
Despite these recent discoveries in the physiological and ecological
proximate factors that control timing of breeding, we still know
22. BEHAVIORAL ECOLOGY OF TROPICAL BIRDS
nothing about the fimess consequences of different individual strate-

gies. There is great variation within a population in breeding strategies,
even though one can presume that the proximate cues experienced
(daylength, rainfall) are virtually identical (Figures 2.2, 2.3). In Song
Wrens, Cyphorinus phaeocephalus, many pairs begin breeding in May, at
the start of the wet season, but other pairs did not lay their first eggs
until September or October (Robinson et al. 2000). The unpredictabil-
ity of tropical breeding seasons at the individual level is illustrated
nicely by White-fronted Bee-eaters, Merops bullockoides, in Kenya
(Wrege and Emlen 1991). Breeding colonies separated by only a few
kilometers breed 6 months apart, during either the long rainy season
(March-May) or the short rainy season (October-December). Within
a colony, neither insect abundance nor rainfall consistently correspond
with time of breeding. Even more puzzling, nests initiated during either
the short rainy season fledge three times as many young as long rainy
season nests. There is no obvious adaptive explanation for why adjacent
colonies breed at different times of the year, but there must be one.
Hypotheses developed to explain temperate zone breeding systems are
inadequate for explaining this kind of tropical phenomenon.
3 Life history traits
It has long been recognized that tropical birds differ fundamentally

from temperate zone birds in their life history traits. Tropical birds have
high nest predation, high adult survival and small clutch sizes (Lack
1947, 1948, 1968, Ricldefs 1969b, Fogden 1972, Skutch 1949).These
characteristics in turn have a big impact on the evolution of other
behaviors such as mate choice and territory acquisition. More recent
studies, however, have questioned the validity of these differences in
tropical birds (Karr et al. 1990, Martin 1996, Geffen and Yom-Tov
2000), causing some confusion and doubt as to whether tropical birds
differ importantly in life history traits. The purpose of this chapter is to
review these debates and determine what life history traits characterize
tropical birds. Others have carefully reviewed the evolutionary
hypotheses to explain why tropical birds are different (Klomp 1970,
Murray 1985, Skutch 1985), so this chapter will summarize what is
known rather than attempt a comprehensive review.
3.1 High nest predation

Early studies of tropical birds typically reported a high percentage of
nests lost to predators, in the order of 80% or more (Snow 1962,Willis
1967, 1972, Fogden 1972, Snow and Snow 1973). In contrast, a pre-
dation frequency of 40-60% is typical of many temperate zone
songbirds (Martin 1993). Some have argued that high nest predation
rates in tropical birds are an artifact of habitat, because a number of the
key studies were done in human-disturbed habitats or islands where
predation rates may be elevated (Oniki 1979, Martin 1996). But recent
studies in large mainland tracts have also found low nesting success
(Robinson et al. 2000). Other studies that question the high nest pre-
dation rate in the tropics have used artificial nests, and found nest
losses in the order of 10-50% (Loiselle and Hopps 1983, Gibbs 1991,
Sieving 1992). Artificial nests often do not reflect true predation fre-
quency (e.g. Wilson and Brittingham 1998), so these alone cannot be
used as evidence for low nest predation in the tropics.
Relatively few studies provide detailed data for nest predation fre-
quency for a large sample of nests of a particular species. A wide
diversity ofpasserines often lose at least 70% of nests (Figure 3.1).This
also applies to many non-passerines, like the Rufous-breasted Hermit,
Glaucis hirsuta (Snow and Snow 1973) and Plain Ground Dove,
Columbina passerina (Oniki 1979). Robinson et al. (2000) found that
only 29% of open-cup nesting forest birds in Panama fledged young.
Predation is the primary cause of nest failure (Ricklefs 1969b). The
percentage of nests lost underestimates nest predation, because this
does not take into account when the nest was first found (many early
nests could have been depredated and therefore never found). Several
studies also used Mayfield's method which estimates daily mortality
rate (Young 1994, Roper and Goldstein 1997, Woodworth 1997,
Robinson et al. 2000). In Dusky Antbirds, Cercomacra tyrannina, only
8% of pairs (15/197) raised young to independence over an eight-year
study, indicating that nesting success must be very low (Morton and
Stutchbury 2000).
Martin (1996) notes some exceptions, tropical species with high
nesting success, but these studies were based on relatively small sample
sizes and are not comparable (Snow and Snow 1963, Skutch 1981).
[] 'Temperate
o~ 4 0 -
v
II Tropical
=o 30-
Ii
10-
o
o 1'o 2o 40
I;I
6'0 7'0 8'0 90
Nest Losses (%)
Figure 3.1
Frequency distribution of predation frequency on nests for studies on north tem-
perate passerines (n = 25, Martin 1993) and Neotropical passerines (n = 9; Snow
1962, Morton 1971b and unpubl, data, Willis 1974, Oniki 1979, Wunderle 1982,
Skutch 1985, Young 1994, Roper and Goldstein 1997, Woodworth 1997). Only
studies with at least 100 nests monitored were included.
LIFE HISTORY TRAITS 25
Nest predation in the tropics likely varies with habitat (Marchant

1960), time of year (Morton 1971b) and possibly altitude (Skutch
1985). Although very high nest predation (> 80% nests) has been
reported for several temperate zone studies (Snow and Snow 1963,
Martin 1993), this is certainly not the norm except in highly disturbed
habitats (e.g. Robinson et al. 1995). For temperate zone passerines the
frequency of nest predation averaged 43.7% (Martin 1993), much
lower than for tropical passerines (Figure 3.1). Robinson et al. (2000),
using a more detailed data set, found that open cup nesting temperate
zone birds averaged 47% nest loss compared with 71% for tropical
birds.
While this s o r t of comparison is very convincing, many of the
tropical species are members of groups that do not have temperate
zone counterparts (antbirds, manakins). Many features of behavior
and life history could influence predation frequency, so a search for real
latitudinal differences owing to habitat should take phylogeny into
account. This is not yet possible because so few tropical species have
been studied in sufficient detail to estimate predation frequency.
A formal comparative analysis not withstanding, we can conclude
that nest predation is higher for most tropical birds. Why is nest preda-
tion so high? It is generally assumed that there is a higher number and
diversity of nest predators in the tropics. Skutch (1949, 1985) sug-
gested that snakes are the primary nest predators, but other studies do
not support this (Roper and Goldstein 1997). Instead, a high abun-
dance and diversity of small mammals, such as mouse opossums,
M a r m o s a sp., in the neotropics, may be implicated as the main predator
species (Roper and Goldstein 1997).
3.2 High adult survival

Snow (1962) was one of the first to show high annual survival (70%) of
adults in a tropical bird, the White-bearded Manakin, M a n a c u s
m a n a c u s . Fogden (1972) did not study any one species intensively, but
reported that 200 of 286 (86%) banded adults of a variety of species
were alive one year later. Willis (1974) reported survival rates of
69-81% for three species of antbirds in Panama, despite two of the
species declining significantly over the study. Most long-term intensive
studies of populations report high adult survival based on resightings
and recaptures of breeders (Table 3.1, reviewed in Sandercock et al.
2000). Such high annual survival rates result in lifespans greater than
10 years being common for these small birds (Snow and Lill 1974,
Table 3.1
Examples of annual survival of territorial adults from population studies of
tropical birds. Superscript '*' indicates survival estimates from recapture data of
known age individuals.
Species Years N Survival (%)
White-bearded Manakin a 9 182 82%

Checker-throated Antwren b 14 40* 75%
Slaty Antshrike c 7 50 54%
Dusky Antbird d 8 25* 82%
Spotted Antbird e 10 >100 81%
Long-tailed Hermit f 4 105 52%
Medium Ground Finchg 16 284 78%
Cactus Ground Finch h 16 210 81%
Hawaii Akepa i 5 82 79%
Long-tailed ManakinJ 8 46 78%
Green-rumped Parrotlet k 10 >500 68%
a: Manacus manacus (Snow 1962, Snow and Lill 1974); b: Myrmotherula fulviventris (Green-
berg and Gradwohl 1997); c: Thamnophilus atrinucha (Greenberg and Gradwohl 1986);
d: Cercomacra tyrannina (Morton and Stutchbury 2000); e: Hylophylax naevioides (Willis
1974); f: Phaethornis superciliosis (Stiles 1992); g: Geospiza fortis (Grant and Grant 1992);
h: Geospiza scandens (Grant and Grant 1992); i: Loxops coccineus (Lepson and Freed 1995);
j: Chiroxiphia linearis (McDonald 1993); k: Forpus passerinus (Sandercock et aL 2000).
Grant and Grant 1992). Willis (1983) recorded three male Spotted
Antbirds, Hylophylax naevioides, over 13 years old. Male Long-tailed
Manakins, Chiroxiphia linearis, do not even begin copulating with
females on the lek until they are nine years old (McDonald 1993).
In surprising contrast, Karr et al. (1990) used capture-recapture
data and Jolly-Seber models to estimate the annual survival of tropical
species to be only 56% (n = 25 species), and concluded they did not
live longer than temperate zone passerines. As noted by Karr et aL
(1990) and others (Martin 1996, Greenberg and Gradwohl 1997,
Johnston et al. 1997, Ricldefs 1997, Sandercock et al. 2000), Karr's
estimates are not comparable to those obtained from breeding birds in
long-term studies. Rather than monitoring known populations, Karr's
data for tropical birds come from routine mist netting of a wide variety
of species in a given locale. Survival estimates are for all banded indi-
viduals regardless of age or territorial status. High dispersal by
juveniles, or the presence of floaters, would result in an underestimate
of true survival (Lepson and Freed 1995). So would territory switching
by adults, common in some tropical birds with year-long territories
(Morton et al. 2001). This is nicely illustrated in the Green-rurnped
Parrotlet, Forpus passerinus (Sandercock et al. 2000), where survival

estimates for non-territorial floaters are much lower than for territorial
breeders (Figure 3.2). For many questions in behavioral ecology, we
are interested in how long a breeder is likely to survive. This affects
decisions about reproductive effort, mate choice and switching territo-
ries. Juvenile survival is important too, but for a different set of
evolutionary questions such as how to acquire territories, and when
and if to disperse.
Figure 3.2
Estimates of survival rate (+ 1 SE) of adult female (n = 485) and male (n = 849)
Green-rumped Parrotlets (Forpus passerinus). Nonbreeders (NB) were individuals
that did not have a nest cavity but were present on the study site, and breeders
(B) were individuals that initiated a clutch. Data from Sandercock et al. (2000).
Johnston et al. (1997) estimated the annual survival of tropical forest

passerines in a long-term mist-netting study in Trinidad to be 65%
(n = 17 species). They used analytical models to remove any bias
caused by young and transient birds in their sample. Even then, they
suggest they have likely underestimated survival. Faaborg and Arendt
(1995) found a survival rate of 68% using capture-recapture data for
9 Puerto Rican passerines. Johnston et al. (1997) used a linear contrast
comparative method to control for phylogenetic effects, and found that
tropical species have a significantly higher annual survival rate than
comparable temperate zone birds.
No matter which method of survival estimation is used (long-term
monitoring of individuals versus capture-recapture), tropical birds
average higher survival than comparable temperate zone birds.
A powerful test is to compare survival in a genus that occurs in both

temperate and tropical regions (unlike manakins, antbirds and
Hawaiian honeycreepers). Ricklefs (1997) used museum collections to
estimate survival ofNewWorld Turdus thrushes to be higher in tropical
(0.76-0.85) than north temperate (0.56) species.
3.3 Small clutch size

Tropical birds do have smaller clutches than temperate zone birds, the
data are unequivocal (Figure 3.3; Cody 1966, Skutch 1985, Kulesza
1990). The prevailing clutch size is 2 eggs for tropical passerines of the
humid neotropics, larger for hole-nesters (Skutch 1985). Within taxo-
nomic groups, clutch size increases two to three fold from the tropics to
high northern latitudes where clutches of 4-6 eggs are common (Cody
1966, Klomp 1970). In the southern hemisphere, the relationship is
weaker or does not exist (Rowley and Russell 1991, Yom-Tov et al.
1994). There are exceptions of course. Some taxonomic groups (Pro-
cellariiforms, hummingbirds, pigeons) do not have latitudinal variation
in clutch size, and some (gannets, crossbills, ravens) show the reverse
trend (reviewed in Klomp 1970). Some tropical birds have an unusually
large clutch, like the Yellow-throated Euphonia, Euphonia hirundinacea,
which lays 5 eggs (Sargent 1993) and the Green-rumped Parrotlet which
lays an average of 7 eggs (Beissinger and Waltman 1991).
While the pattern of small clutches in the tropics is real and uncon-
tested, the evolutionary explanation for this temperate-tropical
difference has been the subject of long debate (Lack 1947, 1948,
Skutch 1949). It is convenient to group these hypotheses into explana-
tions based on immediate costs that limit clutch size versus future
costs. Immediate costs result from tradeoffs between clutch size and
survival of those offspring, and include reduced food delivery to large
broods (Lack 1947, 1948, 1968), increased risk of predation on large
broods (Skutch 1949) and a lower likelihood of juvenile recruitment
with large broods (Young 1996). Future costs are tradeoffs between
current reproductive output and future fecundity and survival, and will
be dealt with in the next section. Both kinds of costs can act to limit
clutch size.
The food limitation hypothesis suggests that latitudinal differences
in daylength allow temperate zone birds to gather more food per day,
thus allowing parents more energy to produce eggs and feed altricial
young (reviewed in Lack 1947, Klomp 1970, Murray 1985). But it is
more than just latitude that affects feeding rates. Growth rates of
Figure 3.3
Clutch size versus latitude for A) the genus Oxyura (stiff-tailed ducks), worldwide
B) the family Tyrannidae (flycatchers), Central and North America C) the genus
Emberiza (sparrows, finches), Africa, Europe and Asia. Data from Cody (1966).
Drawings from Sick (1993), Skutch (1997), and Etchecopar and Hue (1967).
M A T I N G SYSTEMS 55
being insectivorous, the Trumpet Manucode is strictly frugivorous

even when feeding young (Beehler 1985). In contrast to the other birds
of paradise, this species specializes on fig fruit which has low nutritional
value, is relatively uncommon and widely dispersed within the bird's
territory (Beehler 1983). The young may require such a large quantity
of fruit to develop at a normal rate that both parents are needed
(Beehler 1985). Although most birds of paradise are frugivorous and
promiscuous, other frugivorous taxa in New Guinea (cuckoo-shrikes,
honeyeaters, berrypickers) are monogamous (Beehler 1983).
In the Eurylaimidae family endemic to Madagascar, theVelvet Asite,
Philepitta castanea, has a dispersed lek mating system and eats fruit as
well as nectar (Prum and Razafindratsita 1997). Although this is con-
sistent with the fruit-lekking link, two other species in this family form
pair bonds and eat nectar. Why fruit, and not nectar, would be more
likely to promote lekking is not clear. Hummingbirds as a group are
promiscuous and many tropical species have leks (Snow 1974).
These examples show that the connection between diet and promis-
cuity is not as strong as earlier literature suggested. This may be due to
the fact that, no matter how frugivorous adults are, most still feed
insects to their nestlings (Chapter 7). The key to mating system evolu-
tion is not only the diet of adults, but whether females can successfully
breed without male parental care. An important experimental tool to
determine how important male parental care is to reproductive success
is male removal. Most removal studies in temperate monogamous
species have found that male parental care does increase reproductive
success (Wolf et al. 1988). Such experiments have not been done with
tropical species. Do females of insectivorous flycatchers have more dif-
ficulty raising young alone than females of frugivorous flycatchers? Are
male Trumpet Manucodes really needed to raise a brood successfully
on fig fruit alone?
If fruit is so easy to harvest and can be fed to nestlings, why are so
many frugivorous species monogamous? Even in frugivorous birds,
nestlings are often fed arthropods early in their development (Morton
1973). Many frugivores breed during the dry season when arthropod
abundance is low, and male parental care may be crucial only for a few
days when nestlings cannot survive on fruit alone. This could be tested
with temporary male removal experiments in a species like the Clay-
colored Robin where starvation in nestlings is common even when both
parents are feeding (Chapter 3).
4.5 Cooperative breeding

Cooperative breeding, where many individuals can assist a single pair
in breeding or breed together themselves, lies at the other extreme of
sociality from promiscuous species. Cooperative breeding is rare in
north temperate land masses, but is much more common in the tropics
worldwide and Australia (Brown 1987).The first description of helpers
at the nest came from none other than Skutch (1935)! Cooperative
breeders are extremely diverse in terms of taxonomy, habitat, and the
details of the mating system (who helps, how many breeders, etc.), so
searching for underlying ecological determinants of helping behavior is
a challenge. Long-term studies of cooperative breeding have been done
on tropical birds as diverse as the Pied Kingfisher, Ceryle rudis (Reyer
1990), Green Woodhoopoe, Phoeniculus purpureus (Ligon and Ligon
1990), White-fronted Bee-eater, Merops bullockoides (Emlen 1981),
Galapagos Hawk, Buteo galapogoensis (Faaborg 1986), Groove-billed
Ani, Crotophaga sulcirostris (Vehrencamp 1978), and Stripe-backed
Wren, Campylorhynchus nuchalis (Rabenold 1990).
The evolution of cooperative breeding can be understood by exam-
ining two distinct questions (e.g. Brown 1987). First, why do sexually
mature individuals choose to delay breeding and stay home? Second,
why do these individuals then help to raise the young on that territory?
Why stay at home?

As with many other topics discussed in this book, the question can be
turned on its head to ask why cooperative breeding is rare in the tem-
perate zone, rather than why it is common in the tropics. The key
feature of tropical birds that promotes cooperative breeding is perma-
nent residency which allows young birds the option of living with their
parents, or other adults (Brown 1987). Many temperate zone birds are
long distance migrants, which forces young birds to disperse. Individu-
als cannot stay at home if there is no 'home'. There are year-round
residents in the temperate zone, and it is more interesting to consider
why cooperative breeding is not more common among these species.
In resident species, young birds do have the option of staying home,
but under what conditions would this be favored over dispersing and
breeding immediately? High adult longevity is typical of many tropical
birds (Chapter 3) and promotes delayed dispersal in two ways. First,
delayed breeding is a strategy of the future and is more likely to even-
tually pay off for long-lived birds (e.g. Wittenberger 1979). Second,
high adult survival results in a low turnover on territories and few
MATING SYSTEMS 57
breeding vacancies that can be filled by young birds (Brown 1987).

When the production of young exceeds the n u m b e r of breeding vacan-
cies, successful dispersal becomes difficult for most juveniles owing to
habitat saturation.
The habitat saturation model for the evolution of cooperative
breeding is based on the idea that young birds delay dispersal because,
in its strictest form, no breeding habitat is available (Emlen 1982,
Brown 1987).There are several reasons why young may stay home, dis-
cussed by Stacey and Ligon (1991) as 'benefits of philopatry.' Young
may opt to stay home if only marginal or low quality territories are
available, which can be considered another form of habitat saturation
because high quality territories are limiting. In either case, staying
home is more advantageous than dispersing and breeding elsewhere.
This can occur when any critical resource is scarce, including roosting
sites and mates. What evidence is there that habitat saturation actually
occurs in tropical cooperative breeders?
Many studies have demonstrated variation in reproductive success
among groups, and correlated this with some feature of the habitat (e.g.
Langen andVehrencamp 1998).While this implies a likely limitation of
quality territories, it alone is not strong evidence for the habitat satura-
tion model. A stronger approach is to compare populations or species
that differ in mating system, and predict that the cooperatively
breeding populations will experience greater habitat saturation. Zack
and Ligon (1985a,b) compared two species of congeneric shrikes
(Lanius sp.) in Kenya, and found that the cooperative species occupied
dense woodland, a limited habitat with high food abundance during
the dry season that results in high adult survival. These conditions
result in a short supply of high quality territories and few good options
for dispersal for young birds. The non-cooperative species occupies
ubiquitous open habitat with lower food availability, low adult survival,
and abundant breeding territories for young birds. In a unique translo-
cation experiment (Komdeur 1992, K o m d e u r et al. 1995) found that
Seychelles Warblers, Acrocephalus sechellensis, transferred to unoccu-
pied islands showed no cooperative breeding until the high quality
territories were filled. Individuals born on high quality territories were
unlikely to disperse to lower quality territories and instead remained
home to help, but young born on poor territories dispersed to breed on
poor territories.
An experimental test of the 'benefits of philopatry' idea involves the
removal of breeders in territories of differing quality to test whether
vacancies on high quality territories are more likely to get filled quickly.
Zack and Rabenold (1989) found that in Stripe-backedWrens, Campy-

lorhynchus nuchalis, more females fought, and fought more vigorously,
for experimentally created breeding positions in high quality territories
than in low quality territories. In this species territory quality is deter-
mined by group size (number of helpers) rather than an intrinsic
feature of the territory itself.
Resources other than food, such as nest sites and roosting sites, can
also result in limited opportunities for successful dispersal (Restrepo
and Mandrag6n 1998). For instance, cooperative breeding is relatively
uncommon among fruit specialists, perhaps because of the loose terri-
torial system seen in many frugivores owing to the abundance and
changing availability of fruit and the difficulty of defending it (Brown
1987). Cooperative breeding does occur in frugivores like hornbills
(Witmer 1993), and toucan barbets (Restrepo and Mandrag6n 1998),
which defend nesting and roosting cavities.
A limitation of quality territories is not always the answer to delayed
breeding (Macedo and Bianchi 1997). Ecological factors that favor
group living are not restricted to habitat saturation (Koenig and Pitelka
1981), and include group defense of nests (e.g. Cuckoos), group
foraging in anis and cuckoos (Vehrencamp 1978, Macedo and Bianchi
1997), short and unpredictable food supply for raising young so that
helpers are essential (e.g. Bee-eaters), or scattered and clumped food
where group defense is advantageous (e.g. AcornWoodpeckers, Melan-
erpes formicivorus). Nevertheless, the majority of studies on tropical
cooperative breeders have found evidence of a limitation of quality ter-
ritories or mates, which favors delayed dispersal by young (e.g. Emlen
1981, Zack and Rabenold 1989, Ligon and Ligon 1990, Curry and
Grant 1990, Reyer 1990, Strahl and Schmitz 1990).
Why help?
For helping behavior to evolve, young birds must gain some direct or
indirect benefit from helping. In many cooperatively breeding species
the helpers are prior offspring of the breeding pair (reviewed in
Cockburn 1998), suggesting that kin selection can be an important
benefit of helping. But in many species helping by young does not result
in an increased production of nondescendent kin (Cockburn 1998)
and, instead, helpers may benefit directly. In many species helpers end
up breeding on their natal territory, or an adjacent one, indicating that
staying at home is a direct route to breeding independently.
The ecological conditions that favor genetic monogamy in tropical
birds help to set the stage for cooperative breeding to evolve. Indirect
MATING SYSTEMS 59
benefits to helpers are only possible if they are related to the young they
help.While extra-pair paternity affects only who fathers the young on a
territory, even modest levels of EPFs significantly reduces the average
degree of relatedness between helpers and the young they assist. Most
studies of tropical cooperative breeders have found that extra-group
paternity is rare, generally less than 5% ofyoung (Rabenold et al. 1990,
Haydock et al. 1996, Cockburn 1998, Conrad et al. 1998). In some
species, male helpers gain EPFs with the breeding female (within-
group EPFs) but in this case some of the offspring they help are
actually their own (Rabenold et al. 1990) so kin selection does not
apply. The high levels of EPFs found in most temperate species, even
year-round residents, would be an impediment to the evolution of
cooperative breeding.
What kind of help do helpers provide? For many tropical species,
food availability for feeding young appears to be limiting (Chapter 3)
and helpers increase food delivery rates to the nest (e.g. Emlen 1981).
In Pied Kingfishers, Ceryle rudis, (Reyer 1990) unrelated helpers are
tolerated by breeding pairs only in populations with low food supply or
when brood size has been experimentally increased, indicating that
helpers are needed to raise young. Tropical birds also experience high
rates of nest predation (Chapter 3), and helpers in many cooperative
species play a key role in nest defense (Austad and Rabenold 1985,
Innes and Johnston 1996, Restrepo and Mandrag6n 1998).
Why isn't cooperative breeding more common in the tropics?

How well does habitat saturation explain the evolution of cooperative
breeding in the tropics? It is clear that most cooperatively breeding
species experience some form of ecological constraint that favors
delayed dispersal. But, many tropical species that do not breed cooper-
atively nevertheless have the key ingredients that promote cooperative
breeding. These include long lifespan, year-round territoriality, and
variation in territory quality. So why isn't cooperative breeding more
common?
One answer is that the variation in territory quality is not extreme
enough to favor delayed dispersal. This is a sort of 'cooperative
breeding threshold model', akin to the polygyny threshold model that
explains why females should settle polygynously on high quality terri-
tories rather than pair with a monogamous male on a poor quality
territory (Verner andWillson 1966, Orians 1969). Breeding success on
a poor territory must be dismal before kin selection benefits or direct
benefits through inheritance of a good territory can offset the costs of
not breeding at all. Many of the cooperative breeders studied to date

occupy open habitats, which facilitates observation (Brown 1987). But
this bias may also mean that territories vary more in quality, especially
for food abundance during the dry season, than might occur in forest
habitats. Forest birds may not experience sufficient extremes of terri-
tory quality to favor delayed dispersal. This may also apply to resident
temperate zone species, where food abundance during the breeding
season is high for most pairs and raising young is possible on all terri-
tories.
For most tropical birds, those that do not breed cooperatively, little
is known about the variability in territory quality or how (and if)
territory quality affects adult survival and reproductive success.
Furthermore, little is known about the dispersal strategies of young
birds (see Chapter 5). The presence of 'floaters', where young delay
breeding, is good evidence for a limitation of quality territories. In
Rufous-collared Sparrows, Zonotrichia capensis, young birds do delay
breeding but do not help, and instead wait furtively on territories for
vacancies to occur (Smith 1978). In Dusky Antbirds, removal experi-
ments indicated floaters were rare because experimental vacancies
often went unfilled or were filled by neighboring territory owners
rather than previously non-territorial birds (Morton et al. 2000). Com-
parisons of close relatives that differ in cooperative breeding, like Zack
and Rabenold's study on Lanius shrikes in Kenya, are the most promis-
ing way to understand how ecological differences lead to different
mating systems.
5 Territoriality
Latitudinal differences in territorial behavior in relation to breeding

seasons and mating system have had a great influence on latitudinal dif-
ferences in life history strategies. In the temperate zone, territory
establishment by the male, followed by mate attraction is the common
model of territory defense (Freed 1987). Temporary breeding territo-
ries, coupled with high over-winter mortality, mean that males and
females have many unoccupied areas for establishing territories when
they return in spring. For those that do return about 50% of their
neighbors will be altogether new to them. Males and females have very
divergent interests due to the prevalence of extra-pair matings
(Chapter 4). In many species one or both sexes sneak off their territory
to visit neighbors for extra-pair matings (Neudorf et al. 1997, Stutch-
bury 1998b). Females seek out extra-pair matings, whereas males try to
prevent their mates from doing this while at the same time seeking
EPCs themselves. Males must defend their territories from frequent
and sexually-motivated intrusions, even after territory boundaries are
well established. Territorial aggression is highest early in the nesting
season when territories are being established and E P C competition is
at its peak (Arcese 1987).
In the tropics year-long territory defense is common and adult
survival high, so breeding vacancies may be scarce. Consequently,
birds face very different constraints in choosing mates and territories.
It is common that either gender can maintain a territory, if their mate
dies or deserts them, and attract a new mate (e.g. Morton et al. 2000).
Males and females each have similar interests in defending their terri-
tory against same-sexed neighbors, who are after real estate rather than
sex. Actual territorial intrusions are relatively infrequent, but border
disputes and territory defense by singing can persist throughout the
year. Little is known about how territorial aggression varies over the
season, for either gender. Tropical territorial systems are not well
studied, and are much more diverse than the 'simple' year-round
defense described above. The costs and benefits of territory defense
depend on the type of territory and what is at stake. The general
temperate zone model, which is constrained by climate and so driven

by extra-pair mating behavior, applies to only a minority of the tropical
species.
5.1 Territory systems

Over 90% of North American passerines have a similar territorial
system, they defend breeding territories for only a few months each
summer (Table 5.1). In the tropics, as usual, diversity is the name of the
game. Only 13% of passerines defend territories only for the breeding
season. Instead, the predominant territorial system is year-round
defense of feeding and nesting territories (Table 5.1). This territorial
system occurs even in more seasonal habitats such as mangroves
(Lefebvre et al. 1992). The types of resources defended, and when they
are defended, is highly variable in the tropics owing to year-round food
availability and the defensibility, or lack thereof, of different food types.
Generally, insectivores defend year-round all-purpose territories, while
frugivores do not (Morton 1973, Buskirk 1976).Year-round territori-
ality and pair bonding is typical of tropical insectivorous birds, and
occurs in 63% of passerines in Panama (Table. 5.1) and 40% in
tropical South Africa (Rowan 1966). Arthropod resources are defensi-
ble because they are more or less evenly distributed spatially and
temporally.
Table 5.1
Territorial systems of Panamanian passerines compared to North American
passerine birds.
Type o f Territory a Number o f species Number o f genera b

Panama NA Panama NA
Breeding 42 224 28 89
Year-long 142 15 84 13
Army ant influenced 11 0 9 0
Mixed species flock 65 0 40 0
Fruit influenced 43 0 20 0
Lek 28 0 19 0
Total 331 239 200 102
a: See text
b: Species in some genera fit more than one territory type (e.g., Elaenia, Vireo,
Basileuterus, Sporophila).
TERRITORIALITY 63
But there are many variations within this basic pattern. In addition
to year-long territorial and permanent pair bond systems, the tropics
offer:
1. many types of lek and cooperative breeding examples,

2. loosely defended territories where pair members leave well-
defended nesting territories, more or less independently, to visit
fruit sources,
3. species more or less dependent upon the peregrinations of army
ants, and
4. the pros and cons of membership in mixed flocks of several dif-
ferent sorts.
In mixed flocks of the forest interior insectivorous type, many species

are represented by only a pair or small family party. Tanager/flycatcher
flocks of the forest canopy are more frugivorous but might still be rep-
resented by small numbers of each species. In contrast, fruit-eating
birds of more open country, or llanos, characteristically consist of large
groups ofconspecifics (Moynihan 1962, Buskirk 1976, Morton 1979a,
M u n n and Terborgh 1979, Powell 1979). These are discussed further
in Chapter 7.
The amazing diversity of territory types in tropical forests is best
seen by comparing species within the same forest (Figure 5.1). Species
that live in canopy flocks, like the White-shouldered Tanager, Tachy-
phonus luctuosus, have territories about four times the size of species
that live in understory flocks, like the White-flanked Antwren, Myr-
motherula axillaris (Figure 5.1A, B). Obligate ant-following birds like
the Sooty Antbird, Myrmeciza fortis, have huge territories (Figure
5.1 D) compared with other insectivorous birds that defend year-round
territories as pairs or family groups (Figure 5.1C). Lekking species are
common, and either form traditional leks where many males display
very close together (e.g. many hummingbirds and manakins), or they
court as individuals on solitary display perches (Figure 5.1 E) as in the
DwarfTyrant-Manakin, Tyranneutes stolzmanni.
Territory sizes for tropical birds are typically larger than what we see
for comparable birds in the temperate zone (Terborgh et al. 1990). For
instance, forest flycatchers, wrens, robins, tanagers and vireos have ter-
ritories that are typically 5-15 ha in size. This is generally 10 times
larger than the area defended during the breeding season by their tem-
perate zone counterparts (Terborgh et al. 1990). Males and females
each defend the territory against same-sexed challengers, and do not
Figure 5.1
Representative territory types in a floodplain forest in Amazonian Peru
(Terborgh et al. 1990). Shaded areas are territories.
usually cooperate in defending the territory (Greenberg and Gradwohl

1983, Freed 1987, Morton and Derrickson 1996).
Turnover of adults on these territories is very low and this con-
tributes to remarkably stable territory boundaries (Greenberg and
Gradwohl 1997). Lefebvre et al. (1992) suggested that territory stabil-
ity may be low in seasonally versus permanently territorial tropical
species. However, we have found high site fidelity for several species
that seasonally defend nest site territories. Clay-colored Robins, Turdus
grayi, defend territories only during the dry season, and males and
females bred on the same (33/36) or adjacent territory (3/36) in subse-
quent breeding seasons (Stutchbury et al. 1998). Lesser Elaenias,
Elaenia chiriquensis, intratropical migrants that breed in the dry season,
also have high site tenacity with most returning adults renesting on the
same (6/9) or an adjacent (2/9) territory (Morton et al. unpubl). Thus,
TERRITORIALITY 65
territories are stable from the perspective of the individual that reuses
its territory even in species with breeding territoriality. Another con-
tributor to stable neighborhoods is that tropical species with year-long
territories do not expand territorial boundaries, even when given the
opportunity to do so experimentally (Morton et al. 2000). The reason
for this is unstudied, but perhaps birds that are familiar with their ter-
ritories are better able to avoid predators (Lima 1998).
Factors that determine territory quality for tropical birds are little
studied. Food availability during the nonbreeding portion of the year
may be more important in determining territory quality and size than
food during the breeding period. The reason is that breeding success is
often low. A bird might fledge young only once in its life. We speculate
that territory quality will be based upon nonbreeding factors when
annual reproductive success is less than 10%. Then, territorial quality
that increases individual survivorship during periods of low food abun-
dance, often the dry season, will prevail (Morton et al. 2000). Territory
switching in Dusky Antbirds, Cercomacra tyrannina, was related to
increasing adult lifespan and not to reproductive success per se
(Morton et al. 2000).
Interspecific territoriality sometimes occurs where closely related
species (congeners) compete for year-long territories in the most
productive habitats. Robinson and Terborgh (1995) documented
interspecific territoriality using reciprocal heterospecific playbacks in
10 of 12 species of non-oscine passerines in Peru. Most of these had
non-overlapping territories. Some of the same species do not have
interspecific territoriality elsewhere (Stouffer 1997).
Many insectivorous species that are permanently territorial feed in
mixed-species flocks (Powell 1985). It is the foliage-gleaning and bark-
gleaning birds that closely scrutinize substrates that are most tied to
mixed-species flocks, because predator vigilance is difficult to maintain
with this type of foraging (Powell 1985,Thiollay 1999). Mixed-species
flocks allow birds to feed efficiently while taking advantage of the vigi-
lance of the flock (Willis 1972). Generally a flock contains only a single
family group of a particular species, due to strong territoriality. Some
species defend permanent territories smaller in size than the flock, and
the local territory owners join and leave the flock as it moves across ter-
ritory boundaries. This means that a given territorial pair must spend
much time foraging alone on its territory, while the flock is elsewhere.
Other species have territories that conform to the territory boundary of
the multi-species flock (Munn and Terborgh 1979, Power 1979,
Gradwohl and Greenberg 1980). Some species (e.g. antwrens)
sometimes defend seemingly excessive territories, and have very low

population density. This is because the flock's boundaries are deter-
mined by the flock's larger species. Individuals of some smaller species
benefit greatly by defending the entire home range of the flock so that
they can join it at any time.
Other permanently territorial insectivorous passerines are profes-
sional ant-followers (Willis 1967, 1972). The sheer abundance and
spatial concentration of food at ant swarms makes it uneconomical to
exclude conspecifics. Although multiple pairs of a given species may be
present at an ant swarm, the male and female owners of the territory
where the ants are passing through are socially dominant over con-
specifics. As the ants move into a neighboring territory, the owners of
that territory become socially dominant at the swarm.
Many of the 42 species of Panamanian passerines exhibiting
breeding territoriality (Table 5.1) are frugivorous birds, which defend
small nesting territories but feed off-territory on fruiting trees.
However, 13% of the species in Panama are permanently paired and
defend year-long territories but leave them to visit fruit sources. In
Table 5.1 this type of territoriality is called 'Fruit Influenced' to
emphasize that fruit sources are ephemeral and not defended, even
though the bird species have year-long territories and pair bonds (e.g.
Yellow-bellied Elaenia, Elaenia flavogaster) or year-long pair bonds
without year-long territories (e.g. Blue-gray Tanager, Thraupis episco-
pus). This contrasts with army ant influenced territories where pairs
also leave their territories to feed at swarms, because the food supply
(fruit) is not defended by anyone even if it happens to occur within a
pair's territory. For instance, Clay-colored Robin males will not attack
other robins that enter their territory to feed on fruit, but only if the
visitors do not sing while they are there! Many other frugivores lek and
do not even defend nesting territories.
Nectar is defensible because, unlike fruit, the food supply is rapidly
renewed in flowers. In hummingbirds, long-term feeding territories are
usually defended by males only (Wolf 1969, 1975). Intruders, male and
female alike, are chased and attacked vigorously. In several species
males allow females to enter the territory to feed, but only if the females
allows the male to court her. In some species flowers are too scattered
to be defended, so males 'trap-line' by defending a series of high quality
flowers that they revisit on a predictable route.
Why aren't female hummingbirds also territorial? The spatial
concentration of flowers allows males to defend nectar not only
from females, which are smaller, but also from other species of
TERRITORIALITY 67
hummingbirds. This interspecific territoriality means that males can

monopolize high quality flower clusters. Females are forced to feed from
scattered flowers that are not economically defensible. The few hum-
mingbirds where females defend long-term feeding territories feature
bright female coloration (for defense) and are either large so females
can dominate smaller hummingbird species or occur on islands where
there are few interspecific competitors (Wolf 1969, 1975).
Territory defense of food by both sexes, and competition between
the sexes for limited food resources, can drive the evolution of sexual
differences in resource use. The Purple-throated Carib (Eulampisjugu-
laris), a hummingbird, is the sole pollinator of two Heliconia species
(Temeles et al. 2000). Remarkably, specialization by each sex of the
hummingbird on different species of Heliconia has caused sexual
dimorphism in bill size and shape.
5.2 Territory defense

Defense and extra-pair copulations
Territory defense by temperate zone passerines is strongly influenced
by the high frequency of extra-pair matings. In spring, males and
females must acquire or reclaim a breeding territory when they first
arrive. Before the discovery of extra-pair mating systems, much of ter-
ritorial behavior was thought to revolve around establishing and
maintaining the boundaries so neighbors did not take over part of the
territory. Once boundaries are set after a few weeks, strangers (e.g.
floaters) were thought to be a bigger threat to the territory than neigh-
bors (e.g. Wiley 1991). We have a different view of territoriality now.
Males and females make frequent and covert forays onto neighboring
territories, not to take over the territory, but to seek copulations. In
Hooded Warblers, Wilsonia citrina, males and females leave their terri-
tory about once every two hours to sneak onto a neighbor's territory
(Neudorf et al. 1998, Stutchbury 1998b). These are high stake intru-
sions for males, because 20-50% ofyoung are the result of EPCs.There
are winners and losers because some males father many extra-pair
young in addition to those in their own nest, but other males father no
young at all despite having a social mate and feeding the young in her
nest (Stutchbury et al. 1994, 1997). Neighbors are your worst enemy!
Breeding territories are set up nearly simultaneously within a popu-
lation in the temperate zone spring, whereas, most tropical territorial
setting up is not synchronous. Less appreciated is the fact that many of
the differences in territory defense between temperate zone and
tropical passerines are due to influences of extra-pair behavior. In tem-

perate zone passerines, intrusions are a tactic of extra-pair mating
systems. Male territory defense is typically much more vigorous than
female perhaps because females face a greater time tradeoff between
reproduction and territorial behavior (Elekonich 2000). The territorial
system of tropical passerines is based on real estate, because EPCs are
so u n c o m m o n (Chapter 4).
EPCs can be accomplished in a few minutes, so male vigilance
against intruders must be high and persistent. EPC competition means
that intrusion rates are high, and often escalate into fights. In Hooded
Warblers, 20% of covert intrusions resulted in chases or fights with the
territory owner (Stutchbury 1998b). A typical territory owner faces
about one covert intrusion per hour and is involved in at least several
chases or fights per day with intruding males! Even without the aid of
radiotelemetry, such EPC chases are conspicuous and commonly seen
in a wide variety of forest birds.
In tropical passerines actual intrusions onto territories are much less
common (Freed 1987, Greenberg and Gradwohl 1997). Intense fights,
when observed, usually involve take over attempts by juveniles or
floaters, rather than interactions between neighbors. Border disputes,
where single birds or pairs sing at boundaries are common but these
rarely escalate into fights. Pairs of Checker-throated Antwrens, M y r -
motherula fulviventris, for example, defend borders of their mixed
species flock territory against conspecifics with loud and continuous
cheh-cheh-cheh etc. calls accompanied by lateral body movements in
rhythm with the calls. These clashes may last for many minutes.
Male song output is very high in most temperate passerines. It func-
tions in extra-pair mating competition as well as establishing territory
boundaries and attracting a social mate (see Chapter 6). In Hooded
Warblers, males spend about 50% of their time singing even after they
already have a social mate (Wiley et al. 1994, Stutchbury 1998b).
Females assess the quality of potential extra-pair partners by assessing
their singing output and, in some, song variability (Kempenaers et al.
1992, Hasselquist et al. 1996). Mate choice continues long after a male
attracts a social mate to his territory, so males must maintain a high
song output. In most tropical passerines song output is relatively low,
even during the short dawn chorus (see Chapter 6). Many species are
heard only between 0615 and 0730 or for even shorter periods. Some
species have special dawn songs given by males only at or before dawn
(Staicer et al. 1996).
Extra-pair mating also has an impact on territory settlement
TERRITORIALITY 69
patterns. Females prefer to settle on territories where extra-pair males

are nearby (Wagner 1993, 1998,Wagner et al. 1996).This can result in
a clustering of territories with females avoiding settling on territories
isolated from potential extra-pair mates.This is clearly seen in the Least
Flycatcher, Empidonax minimus, which has conspicuous clustering of
tiny territories ('colonies') that shift in location from year to year
(Wagner 1998, S. Tarof, in prep.). The high cost of obtaining EPCs
from isolated territories may explain why so many forest passerines
occur at low frequency in forest fragments that are big enough to
support a breeding pair, but nevertheless are unoccupied (Morton
1992, Norris and Stutchbury 2001). We do not expect to see this EPC-
based territory settlement pattern in tropical passerines.
Testosterone and territoriality

Testosterone is thought to be the key proximate mechanism driving
territory defense in birds. Numerous studies of temperate zone birds
have shown that testosterone level is high during the breeding season,
especially during territory establishment and courtship in spring
(Wingfield et al. 1990). Circulating levels of testosterone correlate with
the individual's current state of aggression only when social relations
are unstable, such as when territories are being established, when the
mate is sexually receptive and when males mate guard (Wingfield et al.
1999). Testosterone levels increase dramatically in individuals chal-
lenged by intruders. Individuals with testosterone implants increase
their territory size (Ketterson et al. 1992). Outside the breeding season,
when gonads are regressed, individuals do not increase testosterone
levels in response to challenges (Wingfield 1994). Wingfield and Hahn
(1994) show that territorial aggression can b e ' activated' in the absence
of testosterone in a sedentary population of Song Sparrows, Melospiza
melodia. However, they insist that persistence of aggression in the face
of a 'simulated territorial intrusion' is still testosterone-dependent
(Wingfield et al. 1999).
Tropical birds break all these rules. Many tropical birds have very
low testosterone levels all year despite being highly aggressive and ter-
ritorial (Dittami and Gwinner 1990, Levin and Wingfield 1992,
Wingfield et al. 1992,Wingfield and Lewis 1993). In Panama, Spotted
Antbird testosterone levels (and gonad size) remain very low year-
round even though individuals defend permanent territories (Figure
5.2; Wikelski et al. 1999a). The seasonal pattern of testosterone is in
sharp contrast with a temperate zone bird like the Red-winged Black-
bird, ,4geliaus phoeniceus (Figure 5.2) or White-crowned Sparrow,
Figure 5.2
Plasma testosterone level (ng m1-1)of male Spotted Antbirds in Panama over the
year, including the breeding season from April-November (from Wikelski et al.
1999a), and for Red-winged Blackbirds in North America that breed from
April-June (Johnsen 1998). Drawings from Medsger (1931) and Wetmore (1972).
Zonotrichia leucophrys (Hau et al. 2000). Testosterone in Spotted

Antbirds became elevated only after prolonged challenges (> 90 min of
playback experiments), whether or not gonads were enlarged, but even
then the maximum ever recorded was 1.5 ng m1-1. This is much lower
than testosterone levels typical of temperate zone birds (4-6 ng ml-1;
Hau et al. 2000). The White-browed Sparrow Weaver, Plocepasser
mahali, in Zambia has a similar low level of testosterone year-round,
but in this species testosterone levels remain low even after simulated
intrusions (Wingfield and Lewis 1992) and experimentally induced
male takeovers (Wingfield et al. 1992).
Either tropical birds do not need testosterone for song and aggres-
sion, or they are highly sensitive to very low levels of testosterone (Hau
et aL 2000). Testosterone implants did increase song and aggression in
captive Spotted Antbirds, and physiological blocking of testosterone
resulted in lower song output and aggression (Hau et al. 2000). This
experiment shows that testosterone can affect song and aggression in
tropical birds, though the T implants increased testosterone levels to
about 6 ng m1-1, much higher than is observed naturally. Such high
TERRITORIALITY 71
levels of testosterone, seen routinely in temperate zone birds, carry a

high price in terms of immunosuppression and other trade offs
(reviewed in Folstad and Karter 1992, Wingfield et al. 1999). Tropical
birds can clearly defend and maintain territories without high testos-
terone levels, and in some species males can elevate testosterone
opportunistically after prolonged territorial challenges (Wikelski et al.
1999a). Such 'social instability' occurs at low frequency in tropical ter-
ritorial systems, largely because males are not competing with each
other for extra-pair copulations (see Chapter 4). Without the strong
sexual selection from extra-behavior there would be no benefit to main-
taining elevated testosterone levels. Females also sing and defend
territories, but nothing is known about the role of testosterone, or other
hormones, in females (Hau et al. 2000).
Resource holding potential

Another tropical/temperate difference concerns the resource holding
potential (RHP) of territory owners. Game theory models of territory
defense distinguish RHP, the physical ability to defend and fight, from
resource value (RV) which is the motivation to fight owing to the value
of the territory to the contestant (Maynard Smith and Parker 1976).
Together, RHP and RV help to predict asymmetries between contes-
tants and therefore the outcome of contests as well as the likelihood of
escalation. These models of territory defense are usually studied exper-
imentally by examining the ability of removed owners to regain their
territories from replacements. Temperate zone removals show that the
probability that replacement individuals will defeat a former resident
increases with replacement time (Krebs 1982, Beletsky 1996). An
absence of 48 h is enough to tip the balance in favor of the replacement,
who is usually a floater rather than a former territory owner. Only 16 %
of Red-winged Blackbird males regained their territory after being
detained for 6-7 d, compared with 91% success in two-day removals
(Beletsky and Orians 1987, 1989).
Few experiments like this have been performed in tropical birds. The
value of breeding territories of temperate zone birds might differ
greatly from the year-long territories of tropical birds. Dusky Antbirds
of either gender always regained their territories, after they were
released from captivity, regardless of replacement time up to 10 days
(Morton et al. 2000). The replacements of the removed territory
owners were other territory owners (not floaters), which switched
mates and old territories for the new territory. The replacements, there-
fore, had the option of returning to the territory they emigrated from
and ousting their replacements, if any. Removed residents, in contrast,

did not have an alternative besides regaining their territory. The
released owners' motivation to fight must have been higher than their
replacements' motivation owing to this asymmetry.
5.3 Territory acquisition

In temperate species, removal experiments have shown that young
birds of many species opt to delay breeding as non-territorial birds,
either because no breeding positions are available (e.g. Stutchbury and
Robertson 1987a, Stutchbury 1991) or in an attempt to gain a high
quality breeding position much as cooperative breeders do (Zack and
Stutchbury 1992). Tactics for gaining territories include wandering
widely for vacancies (Stutchbury and Robertson 1987a), living secretly
(Arcese 1989) or openly (Eckman 1988) on the territories of breeders,
or evicting territory owners outright (Arcese 1987). For most tropical
species removal experiments have rarely been performed (Morton
1977a, Levin 1996a, Morton et al. 2000) and we do not know whether
floaters even exist, let alone how young birds obtain their first territory.
Territory acquisition has been carefully studied in cooperatively
breeding birds, many of them tropical, where young often inherit their
natal territory or use their natal territory as a refuge from which to
compete for breeding positions on nearby territories (Zack 1990).
There are many similarities between cooperative breeders and other
species in how young go about getting a breeding position (Zack and
Stutchbury 1992).
Instead of wandering widely (e.g. 'floating' in the true sense) non-
breeders in some resident temperate species gain a competitive
advantage for breeding vacancies by associating closely with occupied
breeding territories, via the same kind of site dominance advantage that
territory owners enjoy (Birkhead and Clarkson 1985, E c k m a n 1988,
Matthysen 1989). This tactic was first described in a tropical bird, the
Rufous-collared Sparrow, Zonotrichia capensis, in Costa Rica (Smith
1978) where an 'underworld' ofnonbreeders live furtively on the terri-
tories of breeders waiting for a vacancy to arise. Nonbreeders have
well-defined home ranges that they defend from other nonbreeders,
and when a breeder disappears the replacement is a nonbreeder whose
home range included that territory. This kind of nonbreeder tactic for
territory acquisition is likely to be common where year-round territory
defense and high food availability make it possible for young birds to
queue for a breeding position.
TERRITORIALITY 73
In tropical House Wrens, Troglodytes aedon, floaters of both sexes are

transients and have at least two routes to territory acquisition (Freed
1986, 1987). Some wait passively for vacancies to occur, but adults are
long-lived so vacancies arise rarely and are filled very rapidly. Floaters
also attempt to evict territory owners instead of waiting for them to die,
and kill their nestlings if the takeover occurs during breeding. Floaters
sometimes form pair bonds, and then take over territories as a team.
In many monogamous tropical birds, juveniles live on their parent's
territory for several to many months (e.g. Robinson et al. 2000, Morton
et al. 2000), and this could give them an edge in competing for nearby
vacancies that can arise any time of year. In Checker-throated
Antwrens, juveniles live with their parents for a short time (1-2
months), but use this as a home base from which to challenge neigh-
boring territory holders for ownership (Greenberg and Gradwohl
1997). Such challenges involve long contests of displays and chases,
but rarely result in takeovers (unlike House Wrens). Territory acquisi-
tion is constrained by the specialized aerial dead-leaf foraging behavior
of this species. Food resources are scarce within a territory owing to the
limited availability of dead leaves, so young cannot live on their parents'
territory for very long. However, living alone is risky because dead-leaf
foraging makes it difficult to both search for food inside dead leaves
and be vigilant for predators. This species joins mixed-species flocks to
reduce the risk of predation while foraging. Most juveniles that were
banded settled very close to their natal territory.
Spotted Antbird, Hylophylax naevioides, young also leave their
parents' territory after only 6-8 weeks, perhaps owing to competition
with adults at ant swarms. In this species, young birds do not settle near
their parents' territory, and individuals that filled vacancies came from
outside the study area on Pipeline Road, in Panama (J. Nesbitt, pers.
comm.). Many non-territorial 'floaters' that were banded within the
study site eventually acquired breeding territories there, suggesting a
system similar to the 'underworld' described for Rufous-collared
Sparrows (Smith 1978).
In Dusky Antbirds floaters are uncommon, probably because young
birds live with their parents up until the next breeding season and
reproductive success is very low (Morton and Stutchbury 2000,
Morton et al. 2000). Many territories remained unoccupied after an
occupant was experimentally removed during the nonbreeding season,
or when their occupants disappeared naturally. This suggests there is
no shortage of territories. New territories were established by pairs of
juveniles, never by single birds, while 'widowed' adults remained on
their territories and advertised for a new mate to join them (Morton et
al. 2000). In Dusky Antbirds, territory establishment is likely con-
strained by predation. Pairs forage together in dense habitat and do not
join mixed-species flocks, so living alone on a territory may expose a
bird to a very high risk of predation by ambushing predators like vine
snakes and boas.The quality of a territory, to a possible newcomer, may
be greater if an experienced resident is present on it. Such a resident
may be familiar with predators and their locations on the territory. We
predict that, if one removes both residents from a territory, the quality
of that territory will be reduced owing to the high cost of living alone,
and it will remain unoccupied. These total removals can be compared
with published data on replacement rates where only single individuals
were removed (Morton et al. 2000) to test the 'experienced resident
increases territory quality' hypothesis. We present this hypothesis to
stimulate thinking about these tropical territorial systems. Year-long
territoriality is, after all, the most common form of territoriality world-
wide and we know almost nothing about sources of selection acting
upon it.
How juvenile Dusky Antbirds join together to set up territories and
how long they are tolerated on their parents' territories are not well
known. They appeared to form pairbonds with juveniles on adjacent
territories and use space contiguous to both parental territories. In
other words, their territory was budded off a territory from tolerant
parents. When we attempted to capture one such pair for banding, the
mother of one of the paired juveniles left her territory and was
captured! Perhaps she was 'helping out' the daughter.
Other year-round territorial passerines with juvenile retention differ
in some details. Buff-breasted Wren, Thryothorus leucotis, removals
resulted in 100% replacement either by banded young or neighboring
adults, and sometimes unbanded floaters, usually within 24 h (S. Gill
and B. J. M. Stutchbury, unpubl.). Floaters are uncommon, but do
occur. All adults and their young were banded in this population, and
occasionally unbanded birds were observed moving through territories
or singing alone from a small area. In White-bellied Antbirds, Myrme-
ciza longipes, though, experimental removals often did not result in
replacements, suggesting few floaters exist in either sex (B. Fedy and B.
J. M. Stutchbury, unpubl.). These experiments have revealed a great
variety among species that often occupy the same habitats, in terms of
the frequency of floaters, how juveniles go about getting territories, and
how far juveniles go from home to get breeding positions. Why are
White-bellied Antbirds so different from Dusky A n t b i r d s . . . we don't
TERRITORIALITY 75
know! This is so often the answer to questions we, and our students,
pose about tropical birds.
5.4 Territory switching

Year-round territories have remarkably stable boundaries from year to
year, even when owners are replaced (Greenberg and Gradwohl 1986,
1997). But permanent territoriality does not mean stasis. Several
studies have found that territory switching occurs at a low rate in year-
round residents (Willis 1974, Freed 1986, Greenberg and Gradwohl
1986, 1997,Woodworth et al. 1999, Morton et al. 2000).
But switching is an important aspect of territoriality, because the
high adult longevity means that 25-50% of adults switch territories
once during their lifetime (Greenberg and Gradwohl 1997, Morton et
al. 2000). Pair bonds in Dusky Antbirds, apparently stable, are quickly
broken when vacancies arise on nearby territories (Morton et al. 2000).
We removed males or females from territories, then monitored who
filled those vacancies and how quickly this occurred.
Figure 5.3 illustrates how vacancies on some territories are hotly
competed for, while others are ignored. The male from territory A was
replaced by an adjacent male in less than 12 h, which was in turn ousted
by an unbanded male. We then removed the unbanded male and the
same adjacent male moved back to reclaim the vacancy; he was
replaced on his former territory by a yearling neighbor male within
12 h. When the original owner of A was released (after 168 h in captiv-
ity) he reclaimed his territory.The adjacent male returned to his former
territory, as did the yearling male. In stark contrast, a removal on terri-
tory D resulted in no replacements after 70 h, and a natural
disappearance of the male on territory E left that female unmated for
2.5 months!
Territory switching was equally common and rapid among males and
females (Figure 5.4). When the original owners were released they
always won back their territory, and replacements went back to their
former territory, in a domino fashion. On average an individual switched
territories about once in its lifetime. However, some individuals
remained for many years (up to 10) on the same territory, suggesting
these territories were preferred. Territory switching by breeding adults is
probably a common tactic for gaining higher quality territories in many
tropical birds. Levin (1996a) also documented several cases of territory
switching by males and females after doing removal experiments in the
Bay Wren, Thryothorus nigricapillus. In a congener, the Buff-breasted
Figure 5.3
Outcome of male removal experiments (A-D) and one natural disappearance (E)
in the Dusky Antbird during the nonbreeding season (Morton et al. 2000). Terri-
tories (solid lines) are located around the beginning of Pipeline Road, Soberania
National Park, Panama. Dotted lines indicate roads. Arrows indicate source of
replacements (Ub indicates replacement by unbanded male of unknown territory
status). Drawing from Haverschmidt (1968).
Wren, about 15% of adults switch territories during their lifetime,

though some pairs remain together on the same territory for over five
years (S. Gill and B. J. M. Stutchbury, unpubl.).
H o w do adults decide to switch or not to switch territories? H o w do
they assess territory quality on neighboring territories? Direct explo-
ration of the territory is unlikely, and may be too risky if predation risk
is high in unfamiliar terrain. Dusky Antbirds cannot easily leave their
current territory to explore others because the mate they leave, even
for a minute or two, will begin advertising for a new mate if its songs
TERRITORIALITY 11
Figure 5.4
Frequency distribution of time to be replaced for male (n = 9) and female (n = 5)
Dusky Antbirds experimentally removed from territories.
or call notes are not answered (Morton and Derrickson 1996). Song
output, especially during the dawn chorus, does not appear to be an
accurate, if indirect, measure of food abundance on other territories
but the area for foraging was greater in those territories that birds
switched to than it was on those territories they left (Morton et al.
2000).
Mate abandonment is an important aspect of territory switching.
Freed (1986) argued that permanent pair bonds had no intrinsic
benefit in House Wrens, but rather were forced on individuals by the
limited opportunities to switch territories. Switching territories
usually means switching mates also, and the relative benefits to be
gained from each remain unknown. From the practical perspective, it
will be hard to tease apart mate choice from territory choice. In Buff-
breasted Wrens some pairs have remained together, on the same
territory, for over four years (S. Gill and B. J. M Stutchbury, in prep.).
Is this because they are, respectively, high quality mates or because
they both occupy a high quality territory? Perhaps the solution is to
manipulate territory quality through food supplementation, to deter-
mine whether one can induce territory switching. This assumes that
food availability is a key feature of territory quality, and we do not
even know that that is true for tropical birds. Removal experiments
have revealed a wide variety of outcomes, from rapid mate/territory
switching in Dusky Antbirds and Buff-breasted Wrens to very little

mate/territory switching in White-bellied Antbirds. A comparative
approach to explain these differences among species is another way to
determine how important mate and territory quality is for tropical
birds.
6 Communication
6.1 The assessment/management concept in

communication
Communication and its study in animals means different things to dif-
ferent people. For most, communication revolves around the transfer
of information (Owings and Morton 1998). A male who sings is
sending information to his neighbors. Long tail streamers send infor-
mation to females about male quality (Moiler 1988, Andersson 1994).
Readers will be familiar with such informational descriptions because
this perspective has dominated the field. There is a 'sender' and a
'receiver'. Radios transmit information. Computers transmit informa-
tion. Humans, because they have a language, can also transmit
information when they speak. But animals do not talk (Morton and
Page 1992). The information concept is anthropomorphic and does
not do justice to the complex behavioral process that is communica-
tion. In this chapter we will not talk about which signals contain the
most information or how signalers convey information to receivers.
Instead we use a new perspective, the assessment/management concept
(Owings and Morton 1998) to understand and discuss communica-
tion.
Animals communicate because they live in a social world and benefit
from influencing the behavior of rivals, prospective mates, family
members, predators, etc. Let's begin to understand the new perspec-
tive by looking at the sender and the receiver in a communication event.
In the informational view senders are the key participant, it is thought,
because they initiate communication by producing a signal containing
information. In contrast, receivers perceive the signal somewhat pas-
sively then act accordingly, and in their own interest, depending on the
'information' received. But in the new perspective receivers, not
senders, are the more important participant both in the proximate
sense of immediate interactions and in the ultimate sense of how these
cumulatively shape signals through natural selection. Receivers play
the crucial role because they control the outcome of the interaction by
how they respond, if at all, to the signal. Receivers determine what, if

anything, has been accomplished by the signaler. In other words, the
signaler is at the mercy of the receiver. Receivers do not merely absorb
information that is sent their way, they determine, proximately and ulti-
mately, what signals are used and how they are used. We refer to
receivers as 'assessors' to highlight their important role.
Communication signals evolve not to convey information per se, but
as a behavioral mechanism whereby a signaler can attempt to manage,
or regulate, the actions of the assessor so that the signaler benefits from
the interaction. An arms race of sorts, because what is best for the
signaler is not necessarily best for the assessor (and vice versa). Bird
song is an attempt to manage the behavior of another, for instance to
keep an intruder from annexing a portion of a territory. A bird intent on
trespassing into another's territory might ignore the defender's song if
it perceived the singer to be far away. Assessors use sound degradation
to estimate distance (see discussion on ranging below). An assessment
by the would-be intruder that the defender is far away, and hence it is
safe to intrude, becomes a source of selection on songbirds to use songs
that transmit well and appear to be from a closer, more threatening,
defender (Morton 1986, 1996a). A singing bird is not merely sending
information about its location, it is attempting to manage the behavior
of rivals by sounding as close as possible. It can only do this by modify-
ing the way the degradation in its sounds are perceived over distance,
because degradation is the feature by which distance is judged by asses-
sors.
Consider a Dusky Antbird, Cercomacra tyrannina, pair foraging and
duetting at the boundary of a neighbor's territory in their typical
habitat of dense shrubs and grass at the edge of a tropical forest. The
neighboring pair arrives in short order, gives a duet, and soon one
perches close to the threatening pair, fluffs its back feathers (to look
big) and gives a harsh low frequency 'growl.'The foraging pair quickly
retreats. The signal of interest in this case is the growl given at close
proximity to the rival.This is not simply a bird version of'go away'.The
signal given is low frequency and harsh because assessors will be intim-
idated by such signals. Animals assess fighting ability and physical
threat based on size, and a virtually universal rule in communication is
that low frequency sounds come from big animals (Morton 1977b).
Thus, animals from a wide array of taxa use the same low frequency
harsh 'growls' to intimidate, even humans. A person who says 'go away'
in a low frequency harsh tone will sound much more intimidating than
if one uses the exact same words 'go away' but in a high frequency tone
COMMUNICATION 81
(Ohala 1984). Try it. The important point here is that the signals used
in communication depend on how assessments are made; there is more
to it than simply conveying information.
6.2 Song, territoriality and extra-pair behavior

Biologists interested in bird song need to realize that their temperate
zone studies of female mate choice or song function are limited to
'breeding territory' systems (e.g. Moiler 1991, Ratcliffe and Otter
1996, Searcy and Yasakawa 1996 and references therein). Defense of
territories only during the breeding season typifies the vast majority of
temperate zone passerines (Table 5.1). In decided contrast, breeding
season territoriality is u n c o m m o n in tropical passerines and, therefore,
for most bird species. Breeding territoriality was the focus of the
earliest work on avian territoriality, including the work of Eliot
Howard, Bernard Altum, Moffat, and Nice (Stokes 1974), because
these biologists were confined to temperate latitudes. We need much
more work on the other territorial systems found among tropical birds
(Table 5.1) to begin to understand the evolution of territoriality and
how communication is adapted to it.
Singing behavior in temperate zone birds is unique because, due to
climatic constraints, song is highly correlated with territory establish-
ment, pair formation, and breeding. The time devoted to pair
formation and reproduction is a short pulse followed by a long non-
breeding period during which birds stop or reduce territorial behavior,
or migrate out of breeding ranges altogether. In sharp contrast, tropical
territorial behavior and breeding seasons are long-term efforts (Baker
1938). Territories are often defended year-round, and no more inten-
sively during the breeding than the nonbreeding season. Song is used in
territorial defense throughout the year, and pair formation occurs
infrequently and at any time of the year. Furthermore, singing and ter-
ritorial defense are not entirely, or even largely, male behaviors. Other
types of territorial systems are also common in the tropics (Table 5.1).
Song is used year-long among pairmembers of'fruit influenced' terri-
torial species and mixed species flock members. Together with the
standard year-long territorial species, these constitute 76% of the
passerines in some tropical areas (Table 5.1). Clearly, the temperate
zone model does not apply well to these species.
Recent examples continue to overgeneralize about the evolution of
song based on data from breeding territorial systems. These reports,
interesting in their own right, overgeneralize by insisting that bird song
evolves largely as an intersexual form of communication based upon

female choice. Moiler et al. (2000) explain song repertoires of male
birds as resulting from sexual selection because, they suggest, females
prefer males with large repertoires because they suffer less from
malarial parasites, so repertoires reflect health status. While these cor-
relational studies are intriguing, their generality, if any, is limited to
breeding territoriality. They are not generalizable to 'all' bird song
because they do not encompass the diversity of song function in more
c o m m o n territorial systems. What about the 79% of passerines in
Panama alone that have year-long pairbonds? Like the Carolina Wren,
Thryothorus ludovicianus, in N o r t h America, it is not likely that song has
much to do with female mate choice. Instead, this song functions for
defending the territory both inside and out of periods of breeding
(Morton 1996b). For them, the territory is essential for individual
survival throughout the year, not only for reproduction during a
portion of it.
Breeding territoriality contributes to latitudinal differences in the
prevalence of extra-pair mating systems. It is due to this mating system
that song function in temperate zone birds must be viewed as special-
ized and atypical (Chapter 4). In temperate latitudes, males devote
time and energy competing to attract females for EPCs. Testosterone is
the hormone of choice to facilitate the EPC competition amongst
males (Chapter 5). Females actively seek EPCs from neighbors
(Neudorf et al. 1997). If you are a male temperate zone bird your male
neighbor is your worst enemy for you are more likely to lose paternity
to neighbors than to more distant territory holders or nonterritorial
floaters (Stutchbury et al. 1997, Stutchbury 1998b). Most tropical
birds have not evolved extra-pair mating systems (Chapter 4) so their
singing behavior is not influenced by competition for, and defense
against, EPCs.
Song output varies dramatically between tropical and temperate
zone birds because output is a key to females evaluating males for
EPFs. High output, therefore, where a male might be forced to sing to
the point of over-exertion (Morton 1986) is sexually selected. Figure
6.1 illustrates typical song output under an extra-pair mating system in
typical temperate zone birds in contrast to two tropical birds, one with
and one without extra-pair behavior. For most temperate birds with
breeding territories (Mace 1987, Moiler 1991, P~irt 1991, Krokene et
al. 1996, Gil 1999) song peaks sometime between the time of pair for-
mation and incubation, then falls as the breeding season progresses
(Figure 6.1A). The same pattern of singing output occurs in a tropical
COMMUNICATION 83
A. Temperate Zone
80
laredFlycatcher
e-
o..
~ 40
E
I-- ~ ~HoodedWarbler
~ 20
Bluethroat \
i i i I .i .I I i i i i
F M A M J J A S O N D
B. Tropics
80
coloredRobin
o~ 60-
t-
t-
om
00 40-
E
I-.
.~ 20-
Buff-breastedWren
i i i i i i i i i i
J F M A M J J A S 0 N
Figure 6.1
Song output (% time singing) versus time of year for A) typical temperate zone
passerines the Collared Flycatcher Ficeclula albicollis (P~rt 1991), Bluethroat
Luscinia svecica (Krokene eta/. 1996) and Hooded Warbler (Wiley eta/. 1994) and
B) the tropical Clay-colored Robin (Stutchbury et al. 1998) and Buff-breasted
Wren (S. Gill, unpubl).
bird with breeding territoriality and EPFs, the Clay-colored Robin,

Turdus grayi, but in a more typical passerine with year-long territories,
the Buff-breasted Wren, Thryothorus leucotis, song output is very low
and more or less invariable year-round (Figure 6.1B).
Song rate is very low for most tropical passerines, usually less than
one song/minute, even for species that actively defend territories year-
round (Figure 6.2;Wiley and Wiley 1977). The dawn chorus, which is
9 Adelaide's Warbler
[] Buff-breasted Wren
4
A [] Spotted Antbird
r
,,,,,
r
a: 2
O~
r
O
r 1
J F M A M J J A S O N D
Figure 6.2
Variability among neotropical passerines in song rate and seasonality of the dawn
chorus. Data from Staicer et al. (1996), Wikelski et al. (2000) and S. Gill (unpubl.).
when song rate is often highest, still amounts to a paltry 0.5 songs min -1
for Spotted Antbirds, Hylophylax naevioides, even during the breeding
season (Wikelski et al. 2000). White-bellied Antbirds, Myrmeciza
longipes, sing only several times per hour and do not increase song
output even at dawn (Fedy and Stutchbury, unpubl.). The dawn
chorus is impressive in some tropical birds, like the Yellow-bellied
Elaenia, Elaeniaflavogaster, where males sing non-stop for some 15-20
min just before dawn (10-15 songs min -1) during the breeding season,
but pairs sing only 10 times per hour during the daytime (Morton et al.
unpubl.). Adelaide'sWarbler, Dendroica adelaidae, also have a pre-dawn
chorus given during the breeding season that peaks at 4-5 songs min -1
(Figure 6.2), comparable to the song rate of many temperate zone birds
(Moller 1991, P/irt 1991,Titus et al. 1997, Gil et al. 1999). During the
day their song rate is much lower (0.1-1 song min -1) and increases
slightly during the breeding season. Although song rates are typically
very low, for most tropical species singing increases dramatically in
response to playbacks or territorial challenges (Wiley and Wiley 1977,
Levin 1996b, Morton and Derrickson 1996).
If high song output can be used by females to assess males, then
output should reflect differences in male health or vigor and ultimately
in intrinsic male quality (good genes). This has been demonstrated in
several temperate zone species. For instance, female Blackcaps, Sylvia
atricapilla, use song rates rather than territorial quality per se in mating
COMMUNICATION 85
decisions (Hoi-Leitner et al. 1995) as predicted earlier (Morton 1986).

Variation in song output that could be used by females in such evalua-
tions is illustrated by the Clay-Colored Robin (Figure 6.3). Differences
in song output during the dawn chorus could be used by female robins
in choosing males for EPFs (Stutchbury et al. 1998), just as for tem-
perate zone birds.
Figure 6.3
Singing patterns of three individual male Clay-colored Robins (A-C) during the
predawn chorus (0500 to 0600) showing the timing and length of their singing
bouts and sonograms showing their individually recognizable songs. Drawing
from deSchauensee(1964).
The over-riding influence of extra-pair mating systems is seen in

temperate species that are year-round residents (but do not defend ter-
ritories year-round). In Black-capped Chickadees, Poecile atricapillus,
social mate choice occurs gradually and months before breeding
(Smith 1991). Still, females breed synchronously and often choose to
copulate with nonmates (Smith 1988; Otter et al. 1994). Females
assess males for copulation based on song output during the dawn
chorus during the breeding season (Otter et al. 1997) and prefer males
that begin singing earlier, sing longer, and have higher average and
maximal rates. These are usually also males that are high ranking in
winter feeding flocks (Otter et al. 1998) but females, apparently, do not
remember those details and need a more proximate cue to a male's

vigor.
Breeding territories are established nearly simultaneously by most
temperate zone male birds. The competition amongst males is high.
Neighborhoods of birds are highly unstable because territorial bound-
aries are unknown to the many newcomers to the neighborhood. Mate
attraction is also going on, again more or less simultaneously, shortly
after territories are established. Males are forced by female choice to
sing a great deal, which is why food supplementation studies show a
positive influence on song output, and a direct correlation between
song output and female mate preferences, in the temperate zone (Table
6.1). Because they differ in all these respects, tropical birds, those
without extra-pair mating systems, are predicted to sing little relative to
birds of higher latitudes. Food supplementation studies are needed to
test this.
Table 6.1
Studies showing the increase in song output following supplemental feeding.
Species Reference
Pied Flycatcher Alatalo et al. 1990

Ficedula hypoleuca Gottlander 1987
Blackcap Hoi-Leitner et al. 1995
Sylvia atricapilla
Willow Warbler Radesater et al. 1987
Phylloscopus trochilus
Savannah Sparrow Reid 1987
Passerculus sandwichensis
Blackbird Cuthill and Macdonald 1990
Turdus merula
Carolina Wren Morton 1982
Thryothorus ludovicianus Strain and Mumme 1988
Temperate birds might also sing more than tropical birds simply
because they have more food. Carolina Wrens have year-round territo-
ries and do not have EPFs, at least in Alabama (Haggerty et aL in
press). Not only do they respond positively to food provisioning (Table
6.1) but temperate populations sing much more than tropical ones
(Figure 6.4). The temperate zone populations of this wren try to
increase the size of their territories whenever vacancies arise. Those
with larger territories have a better chance of surviving winter snows
COMMUNICATION 87
(Morton and Shalter 1977). Perhaps males sing as much as possible so

as to disrupt the foraging activities of neighbors to better the chances
that vacancies will arise (Morton 1982). Food supplementation studies
have not been performed on tropical birds to see if their song rates are
influenced by food availability. We predict that their singing will not be
influenced by food availability because they sing only to defend real
estate and are not competing for extra-pair matings. Song output
during the dawn chorus in Dusky Antbirds did not increase in birds
whose territories were supplemented with mealworm feeders (Morton
unpubl.).
6.3 Sex role convergence in song

One manifestation of these latitudinal differences is that singing in
female birds is noteworthy in temperate zone birds (Gilbert and
Carroll 1999) but common and characteristic among tropical species
(Morton 1996b). It is clear why females of many tropical species sing;
they are territorial year-round and vigorously defend their territory
from other females. Tropical females are defending food resources for
Figure 6.4
Song rate of male Carolina Wrens outside of the breeding season at different lat-
itudes. Shown are the number of songs given per hour during the dawn chorus,
and the total number of songs given after stimulus by a playback of conspecific
song within the male's territory (data from Morton 1982). Drawing from
Owings and Morton (1998).
themselves and, less importantly for their young, on a permanent basis

or at least for a relatively long time. This favors singing in females as
well as males, not to defend shared territories as a team, but to defend
against competitors of the same sex. Duetting, wherein pair members
sing together, has less to do with the pairbond itself than in insuring
that aggression is used against competitors of the same gender
(Farabaugh 1982). Tropical females can sometimes maintain a year-
long territory even without a mate (Morton et al. 2000). For them, as
in males, songs are better than call notes to manage assessor behavior
over large areas. Sex role convergence occurs due to a need for females,
as well as males, to defend territories (Levin 1996a,b, Morton 1996b).
Female song occurs in some temperate zone species, but is not
always territorial in function. Female Eastern Bluebirds, Sialia sialis,
sing to induce their mates to mob nest predators (Morton et al. 1978)
and female song in other species is associated with coordination of
parental care (Ritchison 1983, Halkin 1997). Females, however, gener-
ally don't sing in the temperate zone. The reasons for this lack of song
are unknown. Territorial defense certainly occurs in temperate zone
species, and females respond to playbacks of female call notes and
attack female mounts (and live intruders!). So why are call notes used
for territory defense instead of song? Singing is costly, and the stakes
are likely lower for temperate females, which defend their territories for
a period of only several weeks. Female defense likely revolves around
preventing settlement by additional females, so that male parental care
for feeding young is guaranteed. Contrast this with tropical females,
who defend critical food supplies that enable them to survive year-
round. Because nesting is synchronous in temperate areas, females can
accomplish territory defense for their short breeding season using
cheaper call notes without the need for the species- and individual-
specificity of song that contributes to male success in extra-pair
competition. Another advantage of using calls, rather than song, is that
nonsinging females do not devote costly brain space to song produc-
tion and perception (Brenowitz et al. 1995, Nealen and Perkel 2000).
The functional role of calls in territory defense is clearly seen in
migrants that defend nonbreeding territories in the tropics. Although
the nonbreeding territories are separated in space from their breeding
territories, these species should rightfully be considered to have year-
long territories. A major difference from their breeding territories,
however, is that both genders defend nonbreeding territories against all
conspecific individuals. Kentucky Warblers, Oporornis formosus, for
example, have typical breeding territories, with males singing and
COMMUNICATION 89
setting up territories, attracting females, and everyone pursuing EPCs.

Later they also defend individual territories during migration and at
overwintering sites in tropical forests (Mabey and M o r t o n 1992) where
species-specific call notes are used to regulate the behavior of all con-
specifics. Neither gender uses song in defense of nonbreeding or
migration territories.The KentuckyWarbler system is used by about 31
species of nearctic migratory passerines, which have both breeding ter-
ritoriality while in eastern N o r t h America and then permanent
territories, while they are in their tropical homes, as do so many other
tropical birds (Morton 1980, Rappole 1995).
In a few temperate species, females do sing to defend nonbreeding
territories but not on their breeding territories, where song is restricted
to males. Song may be favored owing to its long distance propagation
qualities over call notes in these species. The White-eyed Vireo, Vireo
griseus, and European Robin, Erithacus rubecula, are examples. The
vireo requires a source of fruit from the gumbo limbo tree, Bersera
simaruba, on its territory (Greenberg et al. 1995). The tree, of course,
'wants' its fruit eaten so the vireo may be forced to threaten distant con-
specifics to keep them away from the visually obvious attraction of the
fruit. Song would do this better than call notes, which may not carry far
enough.
6.4 Song ranging, neighborhood stability and dialects

Ranging was discovered accidentally. We were trying to capture White-
breasted Wood-wrens, Henicorhina leucosticta, in 1976 along the
Pipeline Road in what is now Parque Nacional Soberania in Panama.
Our goal was to release them on Barro Colorado Island, where these
wrens and other species disappeared from the Island for unknown
reasons. We were looking for the causes of their extirpation (Morton
1978). One way to capture pairs of birds having year-long territoriality
is to play back a tape recording of their songs, making sure to include
duets or examples of both gender's songs, near a mist net placed within
their territory.
We used a high quality recording of duetting White-breasted Wood-
wrens for playback. It came from Cerro Campana, only about 30 km
from the Pipeline Road. Oddly, only male wrens were attracted to the
playback. The males did not react particularly strongly but we were able
to capture enough for the release. When we recorded a local version of
the male song, Pipeline Road males responded much quicker and more
vigorously. Females never showed themselves nor did they utter a
Figure 6.5
Sonogram of the A) duet of a White-breasted Woodwren pair B) a song type
shared by different females in the same Pipeline Road population and C) a differ-
ent song type also shared by females in the Pipeline Road population. Drawing
from Wetmore (1984).
COMMUNICATION 91
sound in response. They completely ignored the duet playback from

Cerro Campana though it contained as much female as male song. We
thought that females must not sing in this population and tucked the
observation away for future study.
A few years later we discovered that female wood-wrens do indeed
sing in the Pipeline Road population (Figure 6.5)! By chance, the male
song version on our Cerro Campana playback tape was similar to one
shared by the local male wrens but the female song was unlike any sung
by the Pipeline Road females. Furthermore, we found that male wood-
wrens each have a large repertoire of ca. 30 songs, most of which are not
identical to songs of neighboring males. In great contrast, female wood-
wrens have only 4 or 5 songtypes and all of these are shared with
neighboring females (Figure 6.5). Male wood-wrens, then, have reper-
toires of songs, mostly unique to individual males (unshared) and
females have a small repertoire of songs that form a dialect. Repertoires
in males, dialects in females have not been described before in song-
birds.
We use the term dialect to refer to contiguous populations with
clearly differentiated vocal patterns, including song neighborhoods
(such as described for Indigo Buntings, Passerina cyanea (Payne 1983))
but not microgeographical variation (Krebs and Kroodsma 1980),
such as that described for the CarolinaWren (Morton 1987).This wren
is typical of most species with repertoires in that neighboring males
share a large percentage (ca. 85%) of their songtypes, but not all of
them, and the percentage of songs shared by males decreases linearly
with distance (Morton 1987). Repertoires and dialects are not
mutually exclusive but there are no known cases of species with more
than about eight songs having all birds in a contiguous population
share all of them as a dialect 'repertoire.' Instead, one sees a gradual
decrease in the percentage of the songs in the repertoires shared among
neighbors with increasing distance between the birds being compared.
The response by male wood-wrens to the Cerro Campana song and
the total lack of response by females to it puzzled us. We began to see a
pattern in other species between responses to playbacks in populations
or species having dialects versus those having large repertoires. Birds
with dialects respond strongly only to their local dialect. Birds with
repertoires respond to any conspecific song. Why? It wasn't until we
read Doug Richards work on Carolina Wrens that we knew the likely
answer. The answer led to a general theory of bird song evolution, the
ranging hypothesis.
Richards (1981) discovered that the key to ranging was the ability of
a listener to use song degradation to estimate its distance from a singer.

Carolina Wrens virtually ignored degraded songs but responded
strongly to these same songs when undegraded versions were broad-
cast at the same volume. H o w did they do this? We suggested that the
assessor must have memorized the song so that it is able to match the
song it hears with the undegraded version it has in its own m e m o r y
( M o r t o n 1982, 1986). In this way it can assess the a m o u n t of degrada-
tion in the song and, because degradation increases with distance, it
can estimate its distance from the singer. It matters little if the song is
from a neighbor or a stranger: as long as the physical structure of the
song is memorized, the listener can range its distance from the singer
no matter who sings it (Falls et al. 1982).
Ranging ties together a lot of 'loose ends' about bird song and its
function and evolution. For example, it explains why birds have evolved
an unusual degree of temporal resolving power even though their
ability to discriminate frequency and intensity changes is not notewor-
thy. A budgerigar can resolve events happening faster than once every
1.2 msec whereas h u m a n s lose sensitivity to events happening faster
than once every 5 or 6 msec (Dooling 1982). Birds are comparable to
echo locating bats with respect to time resolution (Konishi 1969).
Temporal resolving power improves a bird's ranging ability because it
allows them to hear echoes from tree trunks and branches that con-
tribute to degradation in a song as it travels farther and farther from the
singer. Amplitude is probably not useful for ranging because it varies
too much. A singing bird that turns its head away from a listener could
appear to be farther away when, in fact, it hasn't moved, if amplitude
was very important to distance estimation. On the other hand changes
in the frequency mix of a song might also be useful for ranging (Naguib
1995, Fotheringham et al. 1997).
N o wonder White-breasted Wood-wren males did not respond as
strongly to the Cerro C a m p a n a song! They were unable to range the
C a m p a n a song playback because they had no song in their own
m e m o r y to judge it against. But because the males have repertoires,
largely unshared, they responded to the species-specific qualities of the
song. Their response was m u c h stronger once we played back local
songs that added degradation assessment to species-specificity. These
local songs were more threatening and evoked strong territorial aggres-
sion in the males. Female wood-wrens, with their dialects, did not
respond at all and we will discuss why in a m o m e n t .
First, what are dialects and why are dialects favored in some species,
b u t repertoires (and no distinct dialects) favored in others?
COMMUNICATION 93
Temperate/tropical differences in the function of song in territory

defense and mate attraction is closely associated with differences in
repertoire size, individual distinctiveness, and dialects. Tropical species
tend to have stable neighborhoods with long-standing territory bound-
aries known by neighboring territory-holders, and very little active
mate attraction (either social or extra-pair). Temperate species tend to
have unstable neighborhoods with new boundaries established each
year with many new neighbors to compete with, and a very active and
persistent period of mate attraction (first social, then extra-pair).
Ranging theory can explain the effect of neighborhood stability and
mate attraction on repertoire size and dialects. First, we should point
out a major difference in passerine birds that influences songs. Oscines
are often said to 'learn' their songs, because their mature songs are
acquired partly through the experience of hearing them whereas,
because non-oscines do not require such experience, their songs are
described as innate. Obviously such dichotomous terms are shorthand
for the complex developmental interactions that occur during song
acquisition (Marler 1999) but for our purposes this dichotomy is
useful. Oscines, because they learn their songs, can acquire repertoires
with variable amounts of sharing within neighborhoods of competitors,
but many species sing instead but a single song. These single songs
might be completely shared by birds within a population as a dialect, or
be individually distinctive with no dialect. 'Shared' means that one or
more birds sing one or more songs having the same physical structure
such that they sound the same and their spectrograms are identical, or
almost identical. Non-oscine passerines (antbirds, flycatchers, etc.) do
not learn their songs and, consequently, all individuals share the same
song or songs, regardless of whether they have a single song, or a small
repertoire of songs. Non-oscine passerines, which cannot be said to
have dialects because they do not learn songs are, nevertheless, similar
to birds with dialects because neighbors share songs.
The reason some oscines develop single songs and dialects, rather
than flouting their song learning ability by acquiring repertoires, lies in
the stability of their neighborhood. By neighborhood we mean a small
population of birds that can actually hear one another as they defend
territories. The birds interact vocally and try to manage and assess each
other through communication instead of the alternative to communi-
cation, namely fighting. By neighborhood stability, we mean that the
membership in the group of birds that can hear one another changes
relatively little over time.
Neighborhood stability favors the use of songs that can be easily
Fruit is conspicuous and is easily and quickly obtained. As a result,

adults eating fruit have more time to find nestling food. By not eating
invertebrates that might be fed to nestlings, they are not competing
with their own young for this food. It is predictable, then, that most
adult tropical birds do indeed feed invertebrates to their nestlings but
feed themselves on fruit. This can best be seen in relation to territorial
systems (Table 5.1). Species in the 'breeding territory' category include
all the granivores (e.g. Sporophila, Oryzoborus, Jacarina, Tiaris) but also
many adult frugivore species such as Yellow-green Vireo, Vireo (oli-
vaceus) flavoviridis Lesser Elaenia, Elaenia chiriquensis, and Piratic
Flycatcher, Legatus leucophaius, which are intra-tropical migrants
(Morton 1977a). All lekking and all fruit-influenced territorial species
are adult frugivores or total frugivores, as are many of the year-long ter-
ritorial species (e.g. Mimus, all the vireonids, Icterus, Atlapetes,
Arremonops, Saltator, Chlorothraupus, Habia, etc.).
Total frugivory would be common if time/energy budgets for
breeding were the only concern, but they are not. A drawback to fruit-
eating is that it undermines the ability of their nestlings to grow
extraordinarily fast, so fast that it is called the 'altricial nestling
strategy.' Altricial nestling birds, as opposed to precocial ones like
chicks and ducklings, are poikilothermic (cold-blooded) for the first
several days after hatching. Adults brood to maintain the body temper-
ature of their altricial young at or near their own temperature. Energy
from nestling food is fully used by them to grow rather than to regulate
temperature (Dawson and Evans 1957). It is this metabolic saving that
is called the 'altricial strategy,' and it results in nestlings fledging far
faster than would otherwise be possible.
The total frugivore strategy is rare because fruit does not contain
sufficient protein to permit rapid growth and development (Morton
1973). The species that do fit this category can enlarge clutch sizes far
beyond that standard in the tropics, if they have a safe nesting site
(Morton 1973, Sargent 1993), for their parents can gather an unlim-
ited amount of food. However, the time young spend in the nest before
fledging increases as the amount of fruit in the diet increases (Skutch
1954, 1960). Comparative data show this (Figure 7.3). The same is
true for non-oscine passerines (Figure 7.3, Skutch 1969). B. K. Snow
(1970) found that a comparable, totally frugivorous non-oscine, the
Bearded Bellbird, ~ k z s averano, has a lengthy nestling period lasting
33 days.
The altricial nestling strategy is an adaptation for shortening the vul-
nerable period in the nest. This strategy has been particularly valuable
BIOTIC INTERACTIONS 115
Figure 7.3
Average duration of nestling period for total insectivores, adult frugivores and
total frugivores (like the Yellow-crowned Euphonia shown), for oscines and non-
oscines. Data from Skutch (1954, 1960, 1969) and Snow (1970). Drawing from
Skutch (1954).
to passerine birds in allowing them to nest in the 'open' whereas the

nonpasserines, with exceptions, nest in holes affording greater safety.
This gives passerines a flexibility and freedom to nest almost anywhere
(Moynihan 1998). A fruit diet for nestlings cannot sustain the altricial
growth potential with the result that predation pressure will be greater.
In many tropical passerine birds, 75% or more of nests fail to
produce young owing to predation (Ricklefs 1969b). In observing a
75% mortality in a sample of 100 nests, we are left with 25 nests at the
end of a 25-day nesting cycle, which includes incubation and nestling
stages. If this nesting cycle were lengthened by 9 days by frugivory,
another 9.8 nests would be lost to predation, leaving 15.2 successful
nests instead of 25. Dusky Antbirds, Cercomacra tyrannina, may be
typical.Their nests, even with only a 9-day nestling period, have a mere
8% chance of producing independent young (Morton and Stutchbury
2000). Predation imposes a cost on feeding fruit to nestlings and is the
reason why birds do not nourish them with such an abundant food, at
least while they are little and cold-blooded.
But, surely parents would feed fruit to their nestlings if they were
starving! Observations suggest that this is not the case. For example,
nestling starvation was common in Clay-colored Robins, Turdus grayi
(Chapter 2) even though Panax and Miconia berries, figs and papaya,
which were fed to nestlings occasionally, were present in abundance.

By experiment, we found that there is an upper limit to the amount of
fruit nestlings will accept, even when hungry. Captive robin nestlings
(2 days old), after several hours on an all-fruit diet (Bursera simaruba,
Miconia argentea, papaya, banana, figs, palm fruit), still gaped hungrily
for food but refused to swallow more fruit. Crickets, mealworms, and
ground meat were readily accepted by these captives (Morton 1973).
This suggests that, in the wild, nestlings exercise some control over
their diet. Species may vary widely and adaptively in this trait. Two to
four day-old Yellow-bellied, Elaenia flavogaster, and Lesser Elaenias
were fed a mix of fruit (Panax morototoni), tree hoppers, stingless bees,
and some orange spiders about 2.3 m m long. After day six, the
nestlings were fed almost exclusively on fruit (Morton et al. unpubl.).
The highly frugivorous N o r t h e r n Mockingbird, Mimus polyglottus,
does not feed any fruit to nestlings until they have reached the age of
6 days and have begun thermoregulating (Breitwisch et al. 1984).
There is great variation in the timing and amount of fruit fed to
nestlings and almost nothing is known about it. Ecologically important
adjustments to local foraging conditions might occur if adults vary the
proportions of fruit and insects they feed to nestlings over time. That
the tropical fruit/insect strategy is so ubiquitous attests to its success as
a biotic adaptation.
Comparisons of closely related birds nicely illustrate this temper-
ate/tropical difference in b i r d - p l a n t interaction. Contrast the
temperate American Robin, Turdus migratorius, with the tropical Clay-
colored Robin. They are closely related, highly frugivorous as adults,
similar in size, use gardens and lawns for foraging, and have extra-pair
mating systems. American Robins, during their breeding territoriality,
are restricted to invertebrate foods, largely earthworms, and have an
insect/insect adult and nestling diet. After breeding and throughout the
nonbreeding period of the year, they become almost total frugivores
(Wheelwright 1986, Levey and Karasov 1992).They switch to inverte-
brate food during early spring when most overwintering fruit has been
consumed or rotted. When it is cold and earthworms are too deep to
reach, they consume insects that have overwintered as caterpillars,
some of which (e.g. woollybears, Isia isabella) need a great deal of
scraping to remove setae before they can be swallowed (Morton 1968).
Clay-colored Robins also have the breeding territorial system but leave
their territories to feed on fruit. Males and females probably spend only
half of their time on territory rather than nearly all of it as in the
American Robin. Female Clay-colored Robins will travel across a
dozen territories to reach a favorable foraging area to fetch inverte-

brates for their nestlings. Clay-colored robins use a special vocalization
that sounds like skeetch when they are trespassing en route to fruit
sources; the high pitch suggests that it is appeasing to the territory
owner. American Robins have a similar sibilant note that is used as a
'flight call' by birds in frugivorous fall flocks.These thrushes differ only
in the importance fruit has for them while breeding. Their difference
reflects the dissimilar tropical/temperate zone pattern described above.
Latitudinal trends in bird-plant interactions are more complicated
than viewed earlier. It was suggested that plants evolved more nutri-
tious fruits as the dispersal quality of the avian frugivores increased
(Snow 1971, McKey 1975, Howe and Estabrook 1977), a true coevo-
lution with equal tradeoffs between costs and benefits in the birds and
plants. In reality, the idea that birds and plants are coevolved was a
logical suggestion but has not been verified (Herrera 1981). Neither
nutrition of fruits nor the size of the crop and its display seem coevolved
with avian dispersers (Davidar and Morton 1986). The reason for this
is that a third party is involved. It is not simply birds and plants but
predators, birds, and plants that interact (Morton 1973, Howe 1979).
Thus, while avian frugivory has had a huge effect upon the world's
ecology, perhaps because the angiosperms are reproductively superior
to gymnosperms owing to their production of fleshy fruit (Regal 1976),
this effect is likely due to more general biotic interactions than implied
by the term coevolution (Midgley and Bond 1991).
However, plants should do everything they can to lure birds to eat
their fruit and to disperse their seeds. If a plant can produce a laxative
to increase passage rate of seeds to its advantage (Murray et al. 1994),
why not addiction too? Plants have evolved many chemicals to protect
their fruit against rot (Cipollini and Stiles 1993a,b) and birds have
adapted behaviorally (Foster 1987a) and morphologically to a diet of
fruit (Richardson andWooller 1988). So far, although mentioned in the
popular literature (J. Greenberg 1983), no one has documented a plant
that addicts birds to its fruit, even though this would appear possible.
7.3 Biotic interactions and latitudinal adaptations in

migratory birds
Migratory birds, like the two Turdus thrushes, offer examples of
adaptations to tropical and temperate regions. Here we have an oppor-
tunity to compare the same individuals. Migrant birds adapt to all the
regions they inhabit and offer examples of latitudinal changes in the
importance of biotic interactions (Rappole et al. 1983, Rabol 1987).

Even though it was generally thought that most of these migrants leave
the temperate winter because their insect food disappears, nearly all
species become partly or highly or even totally frugivorous during the
tropical portion of their annual cycle. As a whole, the migrant group is
indistinguishable from resident tropical birds in their reliance upon
plants for fruit or nectar while they reside in the tropics (Rappole 1995)
and during migration as well (Parrish 2000).The physiological changes
that accompany this diet switch is a fascinating story in its own right
(Levey and Karasov 1989, Martinez del Rio and Karasov 1990). Even
within the tropics migration is a search for fruit, not insects. All intra-
tropical and elevational migrants travel to find fruit (Levey and Stiles
1992). Yellow-green Vireos and Piratic Flycatchers, for example, leave
breeding territories in Panama in the wet season for dry areas in South
America where fruit is in greater abundance (Morton 1977a). Migra-
tion within and to the tropics, in other words, is based upon the biotic
interactions of plants and birds.
This discovery came as a great shock to some temperate zone com-
munity ecologists, who assumed food habits were consistent during the
year. For example it was mysterious why Cape MayWarblers, Dendroica
tigrina, have fuzzy-tipped tongues, of the sort used to harvest nectar.
They eat insects in the temperate zone. Sure enough, this morphologi-
cal attribute, used rarely in North America (Sealy 1989), fits the
warbler's tropical habits well (Staicer 1992). In Cuba, for example,
Cape Mays are eager nectar and fruit eaters.They are also quite pugna-
cious inter- and intra-specifically. One bird, traveling peacefully with a
flock of resident Terretristis warblers, chased its larger flock mates away
when they began pecking at a 5cm-long red-ripe cactus fruit. Tennessee
Warblers, Vermivora peregrina, gregarious and social when feeding on
insects, become antagonists when feeding on the nectar of Combretum.
Combretum has bright red pollen, which soon coats the heads of
warblers tough enough to defend small patches of this sought-after
plant. Thus 'war painted,' Tennessee Warblers take pollen to new Com-
bretum vines, the red pollen paving the way by marking the dominant
birds.
Similarly, a large tree, Erythrina fusca, attracts Orchard Orioles,
Icterus spurius, to its large leguminous flowers. Orchard Orioles open
the flower 'correctly' by scissoring open the large flag petal, exposing
the nectary and getting pollen on their foreheads in the process. Once
thus opened, a burnt orange color is displayed in the petals surround-
ing the nectary, the same color as that of the dominant male Orchard
Oriole. It is possible that trees with mostly opened flowers signal to

Orchard Orioles that they are occupied and that it would be best for the
birds to find other Erythrina trees, thus dispersing pollen (Morton
1979b).
The Eastern Kingbird, Tyrannus tyrannus, is frugivorous, preferring
the nutritious fruit of Sassafras albidum when leaving its nearctic
breeding areas and Panax morototoni throughout its tropical range
(Morton 1971 a). In fact, this kingbird migrates first to the far southern
end of its nonbreeding range and then moves northwards with the dry
season, apparently tracking the ripening of Panax.
A last example is the red male coloration in Scarlet, Piranga olivacea,
and Summer Tanagers, Piranga rubra. As the scientific name suggests,
Scarlet Tanager males turn olive-green in August before migrating to
South America whereas the male Summer Tanagers retain their red
plumage all year. Scarlet Tanagers are, arguably, even redder than
Summer Tanagers, with a rich scarlet tone as opposed to the Summer
Tanagers' comparatively dull redness. All the carotinoids going into
these bright colors are derived from the birds' diets. We think that the
more brilliant red of the ScarletTanager is derived from its habit of con-
suming the bright red arils found around the seeds of Tetracera spp.
vines. These vines, and, in fact, arils in general, are restricted to the
tropics. Arils are often very nutritious with lipid and protein compo-
nents reaching 60 and 15 percentage of dry weight of the fruits (Foster
and McDiarmid 1983). The Summer Tanager may be restricted to a
dull red by its need to find carotinoids during its temperate zone molt,
which are unlikely to match the red-orange concentrate of Tetracera
arils. When courting a female, a Scarlet Tanager male positions himself
below her, droops his black wings, and displays his incredibly scarlet
back. This should be regarded as a tropical biotic interaction that has
been carried north to continue operating on a temperate breeding ter-
ritory. Such ties to tropical regions underscore the importance of
tropical adaptations to the vast hordes of birds that winter there.
Plants often seem to specialize on migrant birds, perhaps because
they move seeds longer distances than do residents. To attract
migrants, leaves of many of these plants turn red early (e.g. Virginia-
Creeper, Parthenocissus spp.) or have pale or rusty leaf undersides
which flash in the tropical dry season tradewinds (e.g. Cecropea, Panax,
Miconia). The term 'fruit flags' has been applied to describe this adap-
tation for conspicuousness to birds migrating above (E.W. Stiles 1980).
In other cases, migrants eat more fruit than closely related residents.
In the Yucatan Peninsula of Mexico, White-eyed Vireos, Vireo griseus,
migrants from North America, defend individual territories that

overlap extensively with those of the resident Mangrove Vireo, Vireo
pallens. The White-eyed Vireo requires Bursera simaruba trees, whose
fruit ripens slowly over the stay of the vireo from September to April
(Greenberg et al. 1993). It could not overwinter in theYucatan if it were
not for this one tree species (Greenberg et al. 1995). Greenberg (1981)
also found that the red arils of a small tree found on Barro Colorado
Island in Panama, Lindackeria laurina, were only eaten by overwinter-
ing wood warblers (Parulinae). The gregariousness of these birds may
make them important dispersal agents. Such close associations
between nearctic migrant birds and certain tropical plants may be fairly
common.
Indeed, the tropical nonbreeding ranges of many migrant species, or
the overwintering movements of the birds, may be directly related to
locality-specific fruiting patterns (Morton 1980). In central Panama,
Bay-breasted, Dendroica castanea, and Tennessee Warblers moved from
forests during the wet season half of their stay (Oct.-Dec.) to forest
edge where Miconia argentea was a favorite fruit.There they were joined
by Chesmut-sidedWarblers, Dendroica pensylvanica, which abandoned
their forest territories for the fruit (Greenberg 1984a). All species
underwent extensive and rapid molt of body feathers only after the fruit
became available. Because this fruit ripens in the dry season, and the
timing of the dry season in Panama accommodates their molt before
their northward migration, the winter ranges of these warblers may be
influenced by this calendar of seasonal effects on fruit.
While they are in their neotropical ranges, many migrants join mixed
species flocks. There is no suggestion that migrants avoid resident
tropical species that consume foods similar to their own (Table 7.1).
Indeed, the mixed species flocks joined by the most common overwin-
tering warblers and vireos in Panama are found in the canopy, and
these contain the birds most similar to them. Chesmut-sidedWarblers,
Bay-breasted Warblers, Tennessee Warblers, Philadelphia, Vireo
philadelphicus, andYellow-throatedVireos, Vireoflavifrons, are attracted
to flocks led by Lesser Greenlets, Hylophilus minor, the tropical equiva-
lent of the temperate zone chickadees in their attractiveness to flock
participants (Morton 1980). Migrant birds thus are important atten-
dants of tropical mixed species flocks, groups of birds with far more
complexity than found in their temperate zone counterparts.
Table 7.1
Resident species that occur in mixed species flocks in Panama that are joined by
North American migrants (from Morton 1980). Habitat indicates forest canopy,
forest edge or forest understory.
Species Habitat Mass (g)
Plain Xenops Understory 12.0

Checker-throated Antwren Understory 10.4
White-flanked Antwren Understory 8.5
Dot-winged Antwren Understory 11.0
Ruddy-tailed Flycatcher Understory 7.4
Yellow-margined Flycatcher Understory 14.2
Southern Bentbill Understory 6.9
Yellow-green Tyrannulet Canopy 7.0
Forest Elaenia Canopy 12.0
Southern Beardless Tyrannulet Canopy, Edge 6.0
Paltry Tyrannulet Canopy, Edge 7.2
Brown-capped Tyrannulet Canopy, Edge 6.5
Tropical Gnatcatcher Canopy 6.7
Lesser Greenlet Canopy 9.3
Shining Honeycreeper a Canopy, Edge 12.2
Red-legged Honeycreeper a Canopy, Edge 12.0
Green Honeycreeper a Canopy, Edge 13.0
Blue Dacnisa Canopy, Edge 10.0
Fulvous-vented Euphonia a Canopy, Edge 11.5
Golden-hooded Tanager a Canopy, Edge 20.5
White-shouldered Tanager Canopy 13.0
a: Fruit or nectar eating species,joined mainly in dry season.
7.4 Avoiding predators

H o w some cope
Predator avoidance by birds is nearly as diverse as that shown by insects
trying to escape predation by birds. Perhaps it is equally diverse, now
that poisonous birds in the genus Pitohui have been added to the list of
birds suggested to be merely distasteful to predators (Cott 1940).
Pitohuis live in New Guinea yet share a toxin, batrachotoxin, that is
also found in poison dart-frogs (Phyllobates) found in the neotropics
(Dumbacker et al. 1992).
For the majority of tasty birds, however, hiding is a better option.
Studies on lekking birds in the tropics have shown a remarkable degree
of association between plumage color patterns and the exact location
and timing of displays (Endler and Th~ry 1996). This association

results from the ever-present threat of predation. By displaying in
certain light environments, birds can be conspicuous to each other but
not to predators. Let's look in some detail at this example.
Cock-of-the-Rocks display most often mid-morning and mid-after-
noon, and only when the sun is not blocked by clouds (Figure 7.4A).
White-throated Manakins, Corapipo gutturalis, display most often at
mid-day, and usually when the sun is out (Figure 7.4B). The White-
fronted Manakins, Lepidothrix serena, displays most often very early
and late in the day, when the sun is still below the horizon on the
mountain sides where leks occur (Figure 7.4C).When the sun is above
the horizon, males display when clouds block the sun. How do we make
sense of the differences in display behavior between these species? Are
they arbitrary results of sexual selection? No, they reflect behavioral
adaptations to minimize the risk of predation.
The Guianan Cock-of-the-Rock, Rupicola rupicola, is one the most
spectacularly colored neotropical birds, with bright orange body and
white wing strings. Each male defends a small display site consisting of
a horizontal branch about 2 m above the forest floor which is cleared of
leaves below (Endler andTh6ry 1996). Males display when part of their
body is illuminated by a sun speck, and the rest of the body is in shade.
Displays cease when clouds obscure the sun, or when the sun speck
moves off the display site. This display behavior is not arbitrary.
All patches of the plumage pattern (rump and back, strings, light
wing bar) show their maximum reflectance at longer wavelengths. The
forest shade environment where leks are located are rich in these iden-
tical wavelengths. The average overall brightness of the male is least
conspicuous against the visual background during displays, when
males are partially sunlit. A predator viewing the displaying male from
a distance, without discerning individual plumage patches, would have
difficulty picking out the bird against the background. At close range,
the contrast in brightness and hue among the different plumage
patches, and the contrast between the bird and the background, is max-
imized by males displaying partly illuminated by the sun.
The display behavior of the two manakin species also maximizes
their contrast with the background light environment during displays.
MaleWhite-throated Manakins display at the edge of a sun patch, with
their white throat and chest in the sun and their dark back and head in
the shade. They display on a log, and jump between opposite sun
patches when a female arrives. Male White-fronted Manakins have a
turquoise rump patch which is maximally visible in the dark light
Figure 7.4
A) Timing of male lek displays versus time of day in A) Guianan Cock-of-the-Rock
B) White-throated Manakin and C) White-fronted Manakin. Each graph shows
number of observations versus time of day (white bars are sunny conditions, dark
bars are cloudy conditions). For White-fronted Manakin (C) display behavior
differs when sun is belowthe horizon (before 7:30 and after 3:45) compared with
when sun is above the horizon. Figures modified from Endler and Th~ry
(1996). Drawings from de Schauensee and Phelps (1978).
conditions used during display, which also minimizes the visibility of

other body regions.
The color patterns and behavior of birds represents a tradeoff
between crypsis to predators and conspicuousness to conspecifics. The
habitat for lek locations, the times of day to display, and the precise
display behavior are all molded by the constraints imposed by the light
environment. While most easily studied in lekking species where
displays occur at specific sites, these principles apply to all species.
This research has important implications for the conservation of
tropical birds. Display sites are not arbitrary locations, as they might
otherwise seem. The lighting conditions are rather precise, and even
small disturbances on the forest can greatly change the light properties.
A slight disturbance, due to trail construction or selective logging, can
result in abandonment of traditional lek sites (Endler andTh6ry 1996).
It is unknown how important particular light regimes are to territorial
species, as this has never been studied, but one aspect of habitat suit-
ability could include very subtle (to us) lighting conditions that are
crucial for predator avoidance.
How most cope with predators- Mixed Species Flocks

'Wherever one travels on this earth, birds gravitate into mixed foraging
parties. This is true from the shores of the Arctic Ocean to the equator,
in humid forests as well as shrub deserts. The selective forces that
promote aggregative behavior are thus virtually universal and indepen-
dent of climate or vegetation' (Terborgh 1990). Predation on birds by
hawks is commonplace around the world and one common counter-
measure taken by prey species is flocking (Bates 1863, Morse 1970,
1977). In forests, such flocks consist of many species and are termed
mixed species flocks. In open habitats, flocks tend to be monospecific
and often quite large (Morton 1979a). Here, we will not focus on the
anti-predatory nature of flocking but upon its social and ecological
consequences. There are, however, two predatory aspects that deserve
mention in this context. While many eyes are able to detect predators,
so-called 'alarm notes' given by flock members may actually benefit the
caller more than the perceivers (Charnov and Krebs 1975).
Another predation-related aspect is how absorbedly the birds forage.
Tropical birds are generally slow foragers that search intently for
cryptic or hidden prey, compared with temperate zone birds that rely
heavily on caterpillar prey (Figure 7.5). Temperate species most often
glean prey from foliage (Figure 7.5) and forage at a high rate (Thiollay
1988). Tropical passerines feed in wider variety of substrates, using a
wider variety of techniques for prey capture. This basic difference in

food availability and foraging styles has a big impact on social behavior.
Birds that forage intently, for instance by peering inside aerial dead
leaves, can forage best if in company with less intent foragers, such as
those that scan long distances for flying insects (Willis 1972). Which
came first, flocking or intent foraging, is a valid question, but it is true
that dead leaf foragers and others that cannot scan for predators and
forage at the same time are often restricted to mixed species flocks. This
A. Foraging Substrate
70
9 Tropical
[] Temperate
co 40
30
o
10
0 - - "r !
B l - 1 ! !
Foliage Dead Twigs Epiphytes Bark Other

Leaves
B. Mode of Prey Capture
60 /
50 ~ 9 Tropical
o~
40
/ [] Temperate
o
10
0 -- ~ T ,
Glean Probe Snatch Hover Strike Chase
Figure 7.5
Comparison of the overall frequency of occurrence of different foraging sub-
strates and modes of prey capture for tropical passerines in French Guiana and
temperate passerines in France (after Thiollay 1988).
includes some nearctic warblers such as Worm-eating, Helmitheros ver-

mivorus, Blue-winged, Vermivora pinus, Golden-winged, V. chrysoptera,
and Black and White, Mniotilta varia, that join mixed species flocks of
tropical birds consistently if not obligatorily.
While mixed species flocks are found worldwide, like so many other
aspects of avian adaptation, mixed species flocks in the tropics are far
richer in biotic interactions than those in the temperate zone. One
reason for the difference is that flocks are primarily a nonbreeding phe-
nomenon in temperate latitudes. There are no temperate species that
breed in mixed species flocks (Table 5.1). Temperate flocks break down
when their members disperse to breeding territories. Nonetheless,
being in a flock has important consequences even in simple temperate
zone nonbreeding flocks. Flocking can promote efficient foraging
because birds in flocks spend less time on the lookout for predators
than birds alone (Sullivan 1984). But aggression and social dominance
have much to do with where a species typically forages (Morse 1974) as
well as where the individuals within a species feed (Schneider 1984).
There may also be gender differences in foraging such as occurs in the
DownyWoodpecker, Picoides pubescens (Peters and Grubb 1983).
In contrast, tropical mixed species flocks are a dominant feature in
neotropical forests throughout the year (Munn 1985, Powell 1985).
But, although many tropical birds have year-long territoriality
(Chapter 5), those in permanent mixed species flocks are special in that
regard. Their territorial boundaries may overlap to form a shared
boundary for all the regular members of the flock. In Amazonia, mixed
species flocks of the forest understory consist of pairs of 10-20 species.
At least half of these species maintain territories that correspond
exactly to the home range of the entire flock. Powell (1979) notes that
permanent members vary in size, with smaller species occurring at the
same density as larger ones. Single pairs of four small species (8 g body
mass) occupied exclusive territories of 8-12 ha, the same area as
occupied by six larger species (--37 g). Powell suggests that because the
home range is determined by the needs of larger birds, and because the
smaller species exclude conspecifics from the group home range, the
smaller birds must under-utilize the food resources available to them.
This under-utilization, in turn, predicts that smaller species can coexist
with greater niche overlap, resulting in more species diversity of small
species. He tested this idea by comparing the foraging overlap of small
and large species. Sure enough, smaller species had greater foraging
overlap, particularly the three smallest species in the genus Myr-
motherula. Myrmotherula species do differ, however. In Peru, M u n n and
Terborgh (1979) showed that Plain-throated Antwrens, Myrmotherula

hauxwelli, and Pygmy Antwrens, M. brachyura, foraged very low and
very high, respectively. White-eyed Antwrens, M. leucophthalma, and
Ihering's Antwrens, M. iheringi, specialized on dead leaves and the
undersides of vine stems and dead twigs, respectively. Gray Antwrens,
M. menetriesii, foraged higher than the White-flanked, M. axillaris, and
Long-winged Antwrens, M. longipennis, which were similar in foraging
height, techniques, and where they looked.
The frugivore/omnivores tend to be less stable in terms of the indi-
viduals comprising the flocks and they are found mainly in forest
canopy and edge. Many of these have fruit influenced territories and
leave flocks while breeding. Moynihan (1962) studied the 'blue and
green tanager and honeycreeper' flocks, and answered the question of
how the flocks' members stay together. Some species actively follow
others while others are simply followed. Some species contribute to
flock formation, as either followers or those that are followed, while
others do much less to stimulate the formation or maintain the
cohesion of mixed flocks. Moynihan called species that contribute to
flock formation 'nuclear' and others 'attendant.' Others describe 'core'
species, those which occur in all understory flocks and share the jointly
held flock territory. They describe other species with smaller, close-
packed territories, that join a flock when it enters their territory, species
that opportunistically join both canopy and understory flocks and,
lastly, species with patchy foraging habitat that follow flocks regularly
but only as long as they remain within appropriate habitat (Munn and
Terborgh 1979).
The flocks composed of insect-consuming birds are the best studied.
With the exception of ant-following birds, insects are dispersed and
their predators must often work intently to find them or extract them
from hiding places. Predation pressure on insects results in a multitude
of ways and places in which they hide which, in turn, provides different
foraging niches for the birds pursuing them. Thus we have bird species
that glean bark, some that usually sally out from perches, and others
peck inside dead leaves, etc. These birds often occur together and the
different ways and places by which they exploit insects reduces compe-
tition and allows their coexistence in mixed species flocks.
Is this competition scenario true? On the depauperate avifauna of
Cocos Island, 500 km southwest of Costa Rica where only four landbird
species exist, individual Cocos Finches, Pinaroloxias inornata, use spe-
cialized behaviors to exploit insects. Considering the population of
finches as a whole, their range of feeding behaviors span those of several
128 BEHAVIORAL E C O L O G Y OF T R O P I C A L BIRDS
families of birds on the mainland. There are no morphological differ-

ences underlying the foraging specializations, which ranged from
probing or gleaning from leaves, branches or dead leaf clusters to taking
nectar from flowers or extra-floral nectaries to gleaning insects or seeds
from the ground. Instead, each bird may learn the behaviors associated
with its foraging specialty (Werner and Sherry 1987). The foraging
diversity of these Cocos Finches suggests that foraging specialization on
a species level arises when there are many species competing for inver-
tebrate food. Individuals of each species must be better than anyone else
at procuring food in a precise manner. The behavior and the morpho-
logical tools underlying these special skills seem to be based on genetic
differences between species (Greenberg 1983, 1984b, 1987). But the
selection pressure favoring feeding divergence and specialization
Table 7.2
Geographic variation in the average flock size and species richness (total number
of species present, and number of species regularly present) of insectivorous
mixed species flocks in humid low-elevation, humid middle-elevation and dry
tropical forests (from Powell 1985).
,
Location Nucleus Flock Number Number

Speciesa size Species Regulars
Humid-low
Amazonia F 30-35 48 16
Amazonia F 25-30 35 14
Venezuela V - 42 7
Panama F 6 22 5
Panama F - 28 7
Panama F 8 40 7
Panama F 7 34 8
Mexico F-V - 44 -
Honduras F-V 10-15 67 3
Southern Brazil Th - 20 6
Costa Rica F - 31 8
Humid-middle
Panama Th 8-15 21 8
Costa Rica P 8 43 5
Colombia F 22 46 10
Dry
Mexico T 40 10 3
Brazil P - 10 5
a" F, Formicariidae; T, Troglodytidae; V, Vireonida; P, Parulinae; Th, Thraupinae.

probably results from intense territorial behavior. Only those individu-

als that can exclude conspecifics can become the sole member of the
pair of its species within a given flock, and reproduce. The efficiency
with which that individual can obtain food, relative to other con-
specifics, probably has to do with its ability to extract and retain prey in
a mixed species assembly (Graves and Gotelli 1993).
As a result of this potential for foraging specialization on invertebrate
prey, and the addition of omnivores, tropical mixed species flocks can
contain many species. Understory flocks in Peru can contain about 42
species. Total species ranges from 10 to 67 (Powell 1985, Table 7.2).
There have been some reported disadvantages with these large flocks.
Hutto (1988) felt, because the foraging locations and rates of progres-
sion while feeding differed among species, some species must be
making continual adjustments to match the overall rate of flock pro-
gression at the cost of feeding efficiency. Some of the core species are
loud and give alarm calls and some are loud and also steal prey
captured by other flockmates. These activities may be coordinated.The
loud and aggressive White-winged Shrike-tanager, L a n i o versicolor, a
core species in canopy flocks, produces alarm calls to frighten other
birds into dropping their newly captured prey item (Munn 1986).
There is much more to be learned about the social interactions, costs,
and benefits of mixed species flocks in the tropics.
The composition and interactions of flock participants is complex
but flocks are fragile. Flocks disappear when forest structure is changed
or fragmented. The first birds to disappear from fragmented tropical
forests are obligate army ant followers (Willis and Oniki 1978, Lovejoy
et al. 1986).When the forest area is too small to support the army ants,
the birds that depend upon them disappear as well. Moving up from
ant followers at ground level, the mid-level flocks of insectivorous and
the canopy insectivorous and frugivorous flocks degrade or disappear
with habitat alteration (Rappole and Morton 1985). So do those birds
dependent upon the flocks. The destruction or even alteration of a
tropical forest reduces avian biodiversity. But is biodiversity our most
upsetting concern? To us, the answer is no.
7.5 Biodiversity or biotic interactions? What biotic inter-

action means to the conservation of tropical birds
Conservation biologists seem obsessed with the loss of taxa at phylo-
genetic levels above that of the species. Biological diversity, or
biodiversity, is being increasingly viewed as a cladistic phenomenon
(e.g. Nee and May 1997). Biodiversity is measured as the number of

higher taxa (genera) and the total phylogenetic branch length, which is
termed phylogenetic diversity (Purvis et al. 2000). Evolutionary history
is equated with the total length of all the branches of the tree of life.We
feel that something important is missing from this aspect of the loss of
evolutionary history. At one level, what is missing is a feeling for the
adaptations of animals at the species or population level. At another
level, this view implies that what is important is cataloging the existence
of species before they disappear. This has important implications for
how effort is expended in this time of human rampage over the planet.
Latitudinal differences in biotic interactions suggests that conserva-
tion is of paramount importance in tropical regions for a reason rarely
considered by conservationists. Even cladists agree that Darwin's theory
can be applied in the modern world where we can actually see ecological
relationships at work (Gee 1999). The simplification of habitats by
humans will be more devastating in the tropics than in the temperate zone
because biotic interactions have shaped a behavioral and morphological
diversity in tropical birds that is far richer than that found in temperate
zone birds. Biotic interactions produce complex evolutionary results of
the sort most interesting to behavioral ecologists. Understanding these
results within the huge behavioral diversity of tropical birds requires that
the selection pressures underlying the traits can be inferred from current
processes.With the alarming loss and degradation of tropical habitats we
lose not just the individuals of a given species, but also the ability to study
and understand the remarkable adaptations represented through these
species. The adaptations themselves have not been described let alone
the underlying selection balances that produced them. The strong biotic
selection pressures mean that disruption of the environment and loss of
species can quickly erase the evidence necessary to piece together evolu-
tionary processes in the tropics.
This component of evolutionary history is more fragile than the phy-
logenetic branch lengths of cladists and has not been appreciated in
science funding. The research that tropical behavioral ecologists are
producing now will be historically important far beyond its present
value. Recently, behavioral ecologists have begun to realize their
science lacks a foundation in how behavior works, its pragmatic effects.
Will this rising interest in the mechanisms of behavior be thwarted by
the disappearance and distortion of the ecological theater? Surely
research on biotic interactions and behavioral ecology of tropical birds
should be top priority for funding and for positions, but we hear that
Nero did fiddle as Rome burned.
References
Alatalo, R.V., C. Glynn and A. Lundburg. 1990. Singing rate and female
attraction in the pied flycatcher: an experiment. Anim. Behav. 39:
601-603.
Almeida, J. B. and R. H. Macedo. 2001. Lek-like mating system of the
monogamous blue-black grassquit. Auk, in press.
Amundsen, T. 2000.Why are female birds ornamented? Trends Ecol. Evol. 15:
149-155.
Amundsen, T., E. Forsgren and L. T. T. Hansen. 1997. On the function of
female ornaments: male bluethroats prefer colorful females. Proc. Royal
Soc. Lond. B 264:1579-1586.
Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
Arcese, P. 1987. Age, intrusion pressure, and defence against floaters by ter-
ritorial male song sparrows. Anim. Behav. 35: 773-784.
Arcese, P. 1989. Territory acquisition and loss in male song sparrows. Anim.
Behav. 37: 45-55.
Ashmole, N. P. 1963. The regulation of numbers of tropical oceanic birds.
Ibis 103: 458-473.
Austad, S. N. and K. N. Rabenold. 1985. Reproductive enhancement by
helpers and an experimental examination of its mechanism in the bicol-
ored wren: a facultatively communal breeder. Behav. Ecol. Sociobiol. 17:
19-27.
Austen, M. J.W. and P.T. Handford. 1991 .Variation in the songs of breeding
Gambel's white-crowned sparrows near Churchill, Manitoba. Condor
93:147-152.
Bailey, S. F. 1978. Latitudinal gradients in colors and patterns of passerine
birds. Condor 80:372-381.
Baker, J. R. 1938. The relation between latitude and breeding seasons in
birds. Proc. Zool. Soc. A 108: 557-582.
Bancroft, G.T., R. Bowman and R. J. Sawicki. 2000. Rainfall, fruiting phe-
nology, and the nesting season of White-crowned Pigeons in the upper
Florida Keys.Auk 117:416-426.
Baptista, L. F. 1975. Song dialects and demes in sedentary populations of the
white-crowned sparrow, (Zonotrichia leucophrys nuttali). Univ. of California
Publ. Zool. 105: 1-52.
Bates, H.W. 1863. The naturalist on the riverAmazon. Murray, London.
Beecher, M. D., S. E. Campbell, J. M. Burt, C. E. Hill and J. C. Nordby.
2000a. Song-type matching between neighbouring song sparrows. Anim.
Behav. 59:21-27.
Beecher, M. D., S. E. Campbell and J. C. Nordby. 2000b. Territory tenure in
song sparrows is related to song sharing with neighbours, but not to reper-
toire size. Anim. Behav. 59: 29-37.
Beehler, B. 1983. Frugivory and polygamy in birds of paradise. Auk 100:
1-12.
Beehler, B. 1985. Adaptive significance of monogamy in the Trumpet
Manucode Manucodia keraudrenii (Aves: Paradisaeiidae). Ornithol.
Monogr. 37: 83-99.
Beehler, B. and S. G. Pruett-Jones. 1983. Display dispersion and diet of birds
of paradise: a comparison of nine species. Behav. Ecol. Sociobiol. 13:
229-238.
Beissinger, S. R. 1990. Experimental brood manipulations and the mono-
parental threshold in Snail Kites. Amer. Nat. 136: 20-38.
Beissinger, S. R. and J. R. Waltman. 1991. Extraordinary clutch size and
hatching asynchrony of a neotropical parrot. Auk 108:863-871.
Beletsky, L. 1996. The red-winged blackbird, the biology of a strongly polygynous
songbird. Academic Press, San Diego.
Beletsky, L. D. and G. H. Orians. 1987. Territoriality among male red-
winged blackbirds II. Removal experiments and site dominance. Behav.
Ecol. Sociobiol. 20: 339-349.
Beletsky, L. D. and G. H. Orians. 1989a. Territoriality among male red-
winged blackbirds III.Testing hypotheses of territorial dominance. Behav.
Ecol. Sociobiol. 24: 333-339.
Beletsky, L. D., G. H. Orions and J. C. Wingfield. 1989b. Relationships of
steroid hormones and polygyny to territorial status, breeding experience,
and reproductive success in male red-winged blackbirds. Auk 106:
107-117.
Beletsky, L. D., D. F. Gori, S. Freeman and J. C. Wingfield. 1995. Testos-
terone and polygyny in birds. Curr. Ornithol. 12:1-41.
Bennett, A.T.D., I. C. Cuthill, J. C. Partridge and E. J. Maier. 1996. Ultravi-
olet vision and mate choice in zebra finches. Nature 380: 433-435.
Birkhead, T. R. 1998. Sperm competition in birds: mechanisms and function.
Pp 579-622 In: Sperm competition and sexual selection (T.R. Birkhead and
A. P. Moiler, Eds). Academic Press, London.
Birkhead, T. R. and J. D. Biggins. 1987. Reproductive synchrony and extra-
pair copulation in birds. Ethology 74: 320-334.
Birkhead, T. R. and K. Clarkson. 1985. Ceremonial gatherings of the magpie
Pica pica: territory probing and acquisition. Behaviour 94: 324-332.
Birkhead, T. R. and A. P. Moiler. 1992. Sperm competition in birds: evolutionary
causes and consequences. Academic Press, London.
Birkhead, T. R. and A. P. Moiler. 1996. Monogamy and sperm competition in
birds. Pp 323-343 In: Partnerships in birds (J. M. Black, Ed.). Oxford Univ.
Press, Oxford.
Blake, E. R. 1953. Birds of Mexico. Univ. of Chicago Press, Chicago.
Bleiweiss, R. 1985. Iridescent polychromatism in a female hummingbird: Is
REFERENCES 133
it related to feeding strategies? Auk 102: 701-713.

Bleiweiss, R. 1997. Covariation of sexual dichromatism and plumage colours
in lekking and non-lekking birds: a comparative analysis. Evol. Ecol. 11:
217-235.
Boag, P. R. and P. R. Grant. 1984. Darwin's Finches (Geospiza) on Isla
Daphne Major, Galapagos: breeding and feeding ecology in a climatically
variable environment. Ecol. Monogr. 54: 463-489.
Bradbury, J.W. 1981. The evolution of leks. Pp 138-169 In: Natural selection
and social behavior (R. D. Alexander and D. Tinkle, Eds). Chiron Press,
NewYork.
Breitwisch, R., P. G. Merritt and G. H. Whitesides. 1984. Why do Northern
Mockingbirds feed fruit to their nestlings? Condor 86:281-287.
Brenowitz, E. A., K. Lent and D. E. Kroodsma. 1995. Brain space for learned
song in birds develops independently of song learning. J. Neurosci. 15:
6281-6286.
Brown, J. L. 1987. Helping and communal breeding in birds. Princeton Univ.
Press, Princeton.
Brown, J. L., E. R. Brown, J. Sedransk and S. Ritter. 1997. Dominance, age,
and reproductive success in a complex society: a long-term study of the
Mexican jay. Auk 114: 279-286.
Burley, N. 1988. The differential allocation hypothesis: an experimental test.
Amer. Nat. 132:611-628.
Burns, K. 1998. A phylogenetic perspective on the evolution of sexual
dichromatism in tanagers (Thraupidae): the role of female versus male
plumage. Evolution 52:1219-1224.
Buskirk, W. H. 1976. Social systems in a tropical forest avifauna. Amer. Nat.
110:293-310.
Catchpole, C. K. and B. Leisler. 1996. Female aquatic warblers (Acrocephalus
paludicola) are attracted by playback of longer and more complicated
songs. Behaviour 133:1153-1164.
Charnov, E. R. and J. R. Krebs. 1975. The evolution of alarm calls: altruism
or manipulation? Am. Nat. 109:107-112.
Chen, D. M. and T. H. Goldsmith. 1986. Four spectral classes of cone in the
retinas of birds. J. Comp. Phys. A 159: 473-479.
Cipollini, M. L. and E.W. Stiles. 1993a. Fruit rot, antifungal defense, and
palatability of fleshy fruits for frugivorous birds. Ecology 74:751-762.
Cipollini, M. L. and E.W. Stiles. 1993b. Fungi as biotic defense agents of
fleshy fruits: alternative hypotheses, predictions, and evidence. Am. Nat.
141: 663-673.
Cockburn, A. 1998. Evolution of helping behavior in cooperatively breeding
birds. Ann. Rev. Ecol. Syst. 29:141-177.
Cody, M. L. 1966. A general theory of clutch size. Evolution 20:174-184.
Conrad, K. E., M. F. Clarke, R. J. Robertson and P.T. Boag. 1998. Paternity
and the relatedness of helpers in the cooperatively breeding bell miner.
Condor 100: 343-349.
Cott, H. B. 1940. Adaptive coloration in animals. Methuen, London.
Crook, J. H. 1964. The evolution of social organization and visual communi-

cation in weaverbirds (Ploceinae). Behaviour (Suppl) 10:1-178.
Cunningham, E. J. A. and T. R. Birkhead. 1998. Sex roles and sexual selec-
tion.Anita. Behav. 56:1311-1321.
Curry, R. L. and P. R. Grant. 1990. Galapagos mockingbirds: territorial
cooperative breeding in a climatically variable environment. Pp 291-329
In: Cooperative breeding in birds (P. B. Stacey andW. D. Koenig, Eds). Cam-
bridge Univ. Press, Cambridge.
Cuthill, I. C. andW. A. Macdonald. 1990. Experimental manipulation of the
dawn and dusk chorus in the blackbird (Turdus merula). Behav. Ecol. Socio-
biol. 26:209-216.
Cuthill, I. C., A.T.D. Bennett, J. C. Partridge and E. J. Maier. 1999. Plumage
reflectance and the objective assessment of avian sexual dichromatism.
Amer. Nat. 160:183-200.
Davidar, P. 1983. Birds and neotropical mistletoes: effects of seedling
recruitment. Oecologia 60:271-273.
Davidar, P. 1987. Fruit structure in mistletoes and its consequences for seed
dispersal. Biotropica 19:137-139.
Davidar, P. and E. S. Morton. 1986. On the relationship between fruit crop
size and fruit removal by birds. Ecology 76: 262-265.
Davidse, G. and E. S. Morton. 1973. Bird-mediated fruit dispersal in the
tropical genus Lasiacis (Graminae: panicaae). Biotropica 5:162-167.
Dawson, W. R. and F. C. Evans. 1957. Relation of growth and development
to temperature regulation in nestling field and chipping sparrows. Physiol.
Zo61. 30: 315-327.
Deerenberg, C.,V. Arpanius, S. Daan and N. Bos. 1997. Reproductive effort
decreases antibody responsiveness. Proc. Royal Soc. Lond. B 264:
1021-1029.
deSchauensee, R. M. 1964. Birds of Columbia. Livingston Publ. Co. Narberth
PA.
deSchauensee, R. M. and W. H. Phelps, Jr. 1978. A guide to the Birds of
Venezuela. Princeton Univ. Press.
Dittami, J. P. and E. Gwinner. 1990. Endocrine correlates of seasonal repro-
duction and territorial behavior in some tropical passerines. Pp 225-233
In: Endocrinology of birds: molecular to behavioral (M. Wada, Ed.). Japan
Science Society and Springer, Tokyo and Berlin.
Dooling, R. J. 1982. Auditory perception in birds. Pp 95-130 In: Acoustic
communication in birds, vol. 1 (D. E. Kroodsma and E. H. Miller, Eds).
Academic Press, NewYork.
Dumbacker, J. P., B. M. Beehler, T. E Spande, H. M. Garraffo and J.W. Daly.
1992. Homobatrachotoxin in the genus Piwhui: chemical defense in birds?
Science 258:799-801.
Dyrcz, A. 1983. Breeding ecology of the clay-coloured robin Turdus grayi in
lowland Panama. 1his 125: 287-304.
Eckman, J. 1988. Subordination costs and group territoriality in wintering
willow tits. Proc. Int. Ornithol. Congr. 14:2372-2381.
REFERENCES 135
Elekonich, M. M. 2000. Female song sparrow, Melospiza melodia, response to

simulated conspecific and heterospecific intrusion across three seasons.
Anim. Behav. 29:551-557.
Emlen, S.T. 1981. Altruism, kinship, and reciprocity in the White-fronted
Bee-eater. Pp 217-320 In: Natural selection and social behavior (R. D.
Alexander and D. W. Tinkle, Eds). Chiron Press, NewYork.
Emlen, S.T. 1982. The evolution of helping. I. An ecological constraints
model.Amer. Nat. 119: 29-39.
Emlen, S.T. and L.W. Oring. 1977. Ecology, sexual selection, and the evolu-
tion of mating systems. Science 197:215-223.
Emlen, S.T., P. H. Wrege and M. S. Webster. 1998. Cuckoldry as a cost of
polyandry in the sex-role-reversed wattled jacana, Jacana jacana. Proc.
Royal Soc. Lond 265: 2359-2364.
Endler, J. A. 1978. A predator's view of animal color patterns. Evol. Biol. 11:
319-364.
Endler, J.A. and M.Th6ry. 1996. Interacting effects oflek placement, display
behavior, ambient light, and color patterns in three Neotropical forest-
dwelling birds. Amer. Nat. 148:421-452.
Enstrom, D. A. 1993. Female choice for age-specific plumage in the orchard
oriole: implications for delayed plumage maturation. Anim. Behav. 45:
435-442.
Estrada, A. and T. Fleming. 1985. Frugivores and seed dispersal. Junk, The
Hague.
Etchecopar, R. D. and F. Hue. 1967. The Birds of NorthAfrica. Oliver & Boyd,
London.
Evans Ogden, L. G. and B. J. M. Stutchbury. 1996. Constraints on double
brooding in a neotropical migrant, the Hooded Warbler. Condor 98:
736-744.
Evans Ogden, L .G. and B. J. M. Stutchbury. 1997. Fledgling care and male
parental effort in the Hooded Warbler (Wilsonia citrina). Can. J. Zool. 75:
576-581.
Faaborg, J. 1986. Reproductive success and survivorship in the Galapagos
Hawk, Buteo galapagoensis: potential costs and benefits of cooperative
polyandry. Ibis 128: 337-347.
Faaborg, J. and W. J. Arendt. 1995. Survival rates of Puerto Rican birds: are
islands really that different? Auk 112: 503-507.
Falls, J. B., J. R. Krebs and P. K. Mcgregor. 1982. Song matching in the Great
tit (Parus major): the effect of similarity and familiarity. Anita. Behav. 30:
977-1009.
Farabaugh, S. M. 1982.The ecological and social significance ofduetting. Pp
85-124 In: Acoustic communication in birds (D. E. Kroodsma and E. H.
Miller, Eds). Academic Press, NewYork.
Feekes, F. 1981. Biology and colonial organization of two sympatric
caciques, Cacicus c. cela and Cacicus h. haemorrhous (Icteridae, Aves) in
Surinam. Ardea 69: 83-107.
Fleischer, R. C., C. Tarr and T. K. Pratt. 1994. Genetic structure and mating
system in the palila, an endangered Hawaiian honeycreeper, as assessed by

DNA fingerprinting. Molecular Ecology 3: 383-392.
Fleischer, R. C., C. Tarr, E. S. Morton, K. D. Derrickson and A. Sangmeis-
ter. 1997. Mating system of the Dusky Antbird (Cercomacra tyrannina), a
tropical passerine, as assessed by DNA fingerprinting. Condor 99:
512-514.
Fleming, T. H., R. Breitswich and G. H. Whitesides. 1987. Patterns of
tropical vertebrate diversity. Ann. Rev. Ecol. Syst. 18:91-109.
Fogden, M. P. L. 1972.The seasonality and population dynamics of equato-
rial forest birds in Sarawak. Ibis 114: 307-343.
Folstad, I. and A. J. Karter. 1992. Parasites, bright males, and the immuno-
competence handicap. Amer. Nat. 139: 603-622.
Forsyth, A. and K. Miyata. 1984. Tropical nature. Life and death in the rain-
forests of Central and South America. Simon and Schuster Publ., NewYork.
Foster, M. S. 1974.A model to explain molt-breeding overlap and clutch size
in some tropical birds. Evolution 28:182-190.
Foster, M. S. 1975. The overlap of molting and breeding in some tropical
birds. Condor 77:304-314.
Foster, M. S. 1981. Cooperative behavior and social organization of the
Swallow-tailed Manakin (Chiroxiphia caudata). Behav. Ecol. Sociobiol. 9:
167-177.
Foster, M. S. 1987a. Feeding methods and efficiencies of selected frugivo-
rous birds. Condor 89: 566-580.
Foster, M. S. 1987b. Delayed maturation, neoteny, and social system differ-
ences in two manakins of the genus Chiroxiphia. Evolution 41" 547-558.
Foster, M. and R. W. McDiarmid. 1983. Nutritional value of the aril of
Trichilia cuneata, a bird-dispersed fruit. Biotropica 15:26-31.
Foster, R. B. 1982. The seasonal rhythm of fruitfall on Barro Colorado
Island. In: The ecology of a tropical rainforest (E. G. Leigh, Jr., A. S. Rand and
D. M.Windsor, Eds). Smithsonian Inst. Press, Washington.
Fotheringham, J. R., P. R. Martin and L. Ratcliffe. 1997. Song transmission
and auditory perception of distance in wood warblers (Parulinae). Anim.
Behav. 53: 1271-1285.
Freed, L. A. 1986. Territory takeover and sexually selected infanticide in
tropical house wrens. Behav. Ecol. Sociobiol. 19:197-206.
Freed, L. A. 1987. The long-term pair bond of tropical house wrens: advan-
tage or constraint? Amer. Nat. 130: 507-525.
Fuentes, M. 1992. Latitudinal and elevational variation in fruiting phenology
among western European bird-dispersed plants. Ecography 15:177-183.
Gee, H. 1999. In search of deep time: beyond the fossil record to a new history of
life. The Free Press, NewYork.
Geffen, E. andY.Yom-Tov. 2000. Are incubation and fledging periods longer
in the tropics? J.Anim. Ecol. 69: 59-73.
Gibbs, J. P. 1991. Avian nest predation in tropical wet forest: an experimen-
tal study. Oikos 60:155-161.
Gil, D., J. A. Graves and P. J. B. Slater. 1999. Seasonal patterns of singing in
REFERENCES 137
the willow warbler: evidence against the fertility announcement hypothe-

sis. Anim. Behav. 58: 995-1000.
Gilbert, W. M. and A. E Carroll. 1999. Singing in a mated female Wilson's
Warbler. Wilson Bull. 111: 134-137.
Gottlander, K. 1987. Variation in the song rate of the male pied flycatcher
(Ficedula hypoleuca): causes and consequences. Anim. Behav. 35:
1037-1043.
Gradwhol, J. and R. Greenberg. 1980. The formation of antwren flocks on
Barro Colorado Island, Panama. Auk 97: 385-395.
Gradwohl, J. and R. Greenberg. 1982. The breeding season of antwrens on
Barro Colorado Island. Pp 345-351. In: The ecology of a tropical rainforest
(E. G. Leigh, Jr., A. S. Rand and D. M. Windsor, Eds). Smithsonian Inst.
Press, Washington.
Grant, P. R. and B. R. Grant. 1992. Demography and the genetically effective
sizes of two populations of Darwin's Finches. Ecology 73: 766-784.
Graves, G. R. and N. J. Gotelli. 1993. Assembly of avian mixed-species flocks
in Amazonia. Proc. Natl.Acad. Sci. USA 90:1388-1391.
Greenberg, J. 1983. Natural highs in natural habitats. Science News 124:
300-301.
Greenberg, R. 1981. Frugivory in some migrant tropical forest wood
warblers. Biotropica 13:215-223.
Greenberg, R. 1983. The role of neophobia in determining the degree of
foraging specialization in some migrant warblers. Am. Nat. 122: 444-453.
Greenberg, R. 1984a. The winter exploitation system of Bay-breasted and
Chesmut-sided Warblers in Panama. Univ. Calif. Publ. Zool. 116. Univer-
sity of California Press, Berkeley.
Greenberg, R. 1984b. The role of neophobia in the foraging selection of a
tropical migrant bird: an experimental study. Proc. Natl.Acad. Sci USA 81:
3778-3780.
Greenberg, R. 1987. Development of dead leaf foraging in a tropical migrant
warbler. Ecology 68:130-141.
Greenberg, R. and J. Gradwohl. 1983. Sexual roles in the Dot-winged
Antwren (Microrhopias quixensis), a tropical forest passerine. Auk 100:
920-925.
Greenberg, R. and J. Gradwohl. 1986. Constant density and stable territori-
ality in some tropical insectivorous birds. Oecologia 69:618-625.
Greenberg, R. and J. Gradwohl. 1997. Territoriality, adult survival, and dis-
persal in the Checker-throated Antwren in Panama. J. Avian. Biol. 28:
103-110.
Greenberg, R., D. K. Niven, S. Hopp and C. Boone. 1993. Frugivory and
coexistence in a resident and a migratory vireo on theYucatan Peninsula.
Condor95: 990-999.
Greenberg, R., M. Foster and L. Marquez. 1995. The role of White-eyed
Vireos in the dispersal ofBursera simaruba fruit. J. Trop. Ecol. 11:619-639.
Griscom, L. and A. Sprunt. 1957. The warblers ofAmerica. Devin-Adair Co.,
NewYork.
Haggerty, T., E. S. Morton and R. C. Fleischer. 2001. Genetic monogamy in

the CarolinaWren, Thryothorus ludovicianus.Auk, in press.
Hails, C.J. 1982. A comparison of tropical and temperate aerial insect abun-
dance. Biotropica 14:310-313.
Halkin, S. L. 1997. Nest-vicinity song exchanges may coordinate biparental
care of northern cardinals. Anim. Behav. 54:189-198.
Hamilton, W. D. and M. Zuk. 1982. Heritable true fitness and bright birds: a
role for parasites? Science 218: 384-387.
Hansen, A. J. and S. Rohwer. 1986. Coverable badges and resource defence
in birds.Anim. Behav. 34: 69-76.
Harris, M. P. 1970. Breeding ecology of the Swallow-tailed Gull, Creagrus
furcatus.Auk 87: 215-243.
Harris, M. A. and R. E. Lemon. 1974. Songs of Song Sparrows (Melospiza
melodia): individual variation and dialects. Can. J. Zool. 50:301-309.
Hasselquist, D., S. Bensch and T. von Schantz. 1996. Correlation between
song repertoire, extra-pair paternity and offspring survival in the great
reed warbler. Nature 381: 229-232.
Hasselquist, D., J. A. Marsh, P.W. Sherman, and J. C. Wingfield. 1999. Is
avian humoral immunocompetence suppressed by testosterone? Behav.
Ecol. Sociobiol. 45:167-175.
Hau, M., M.Wikelski and J. C.Wingfield. 1998. A neotropical forest bird can
measure the slight changes in tropical photoperiod. Proc. R. Soc. Lond. B
265: 89-95.
Hau, M., M. Wikelski, K. K. Soma and J. C. Wingfield. 2000. Testosterone
and year-round territorial aggression in a tropical bird. Gen. Comp.
Endocrinol. 117: 20-33.
Haverschmidt, F. 1968. Birds of Surinam. Oliver and Boyd, London.
Haydock, J., P. G. Parker and K. N. Rabenold. 1996. Extra-pair paternity is
uncommon in the cooperatively breeding Bicolored Wren. Behav. Ecol.
Sociobiol. 38:1-16.
Herrera, C. M. 1981. Are tropical fruits more rewarding to their dispersers
than temperate ones? Am. Nat. 118: 896-907.
Hill, G. E. 1990. Female house finches prefer colourful males: sexual selec-
tion for a condition-dependent trait. Anim. Behav. 40: 563-572.
Hill, G. E. 1993. Male mate choice and the evolution of female plumage col-
oration in the House Finch. Evolution 47: 1515-1525.
Hoi, H. 1997. Assessment of the quality of copulation partners in the monog-
amous bearded tit. Anim. Behav. 53: 277-286.
Hoi, H. and M. Hoi-Leimer. 1997. An alternative route to coloniality in the
bearded tit: females pursue extra-pair fertilizations. Behav. Ecol. 8:
113-119.
Hoi-Leimer, M., H. Nechtelberger and H. Hoi. 1995. Song rate as a signal
for nest site quality in blackcaps (Sylvia atricapilla). Behav. Ecol. Sociobiol.
37: 399-405.
Holmes, R. T. and J. C. Schultz. 1988. Food availability for forest birds:
effects of prey distribution and abundance on bird foraging. Can. J. Zool.
REFERENCES 139
66: 720-728.
Holmes, R. T., T. W. Sherry and F. W. Sturges. 1986. Bird community
dynamics in a temperate deciduous forest: long-term trends at Hubbard
Brook. Ecol. Monogr. 56:201-220.
Howe, H. F. 1979. Fear and frugivory. Am. Nat. 114:925-931.
Howe, H. F. and G. F. Estabrook. 1977. On intraspecific competition for
avian dispersers in tropical trees.Am. Nat. 111: 817-832.
Howe, H. F. and J. SmaUwood. 1982. Ecology of seed dispersal. Ann. Rev.
EcoL Syst. 13:201-228.
Hunt, S., I. C. Cuthill, A. T. D. Bennett and R. Griffiths. 1999. Preferences
for ultraviolet partners in the blue tit. Anirn. Behav. 58:809-815.
Hutchinson, G. E. 1965. The ecological theater and the evolutionary play. Yale
University Press, New Haven.
Hutto, R. L. 1988. Foraging behavior patterns suggest a possible cost associ-
ated with participation in mixed-species flocks. Oikos 51: 79-83.
Innes, K. E. and R. E. Johnston. 1996. Cooperative breeding in the white-
throated magpie-jay. How do auxiliaries influence nesting success? Anirn.
Behav. 51: 519-533.
Irwin, R. E. 1994.The evolution of plumage dichromatism in the NewWorld
blackbirds: social selection on female brightness? Amen. Nat. 144:
890-907.
Isler, M. L. and P. R. Isler. 1999. The Tanagers. Smithsonian Inst. Press.,
Washington.
Janzen, D. H. 1969. Birds and the ant x acacia interaction in Central
America, with notes on birds and other myrmecophytes. Condor 71:
240-256.
Janzen, D. H. 1973. Sweep samples of tropical foliage insects: description of
study sites with data on species abundances and size distributions. Ecology
54: 659-686.
Janzen, D. H. 1975. Ecology ofplants in the tropics. Edward Arnold, London.
Janzen, D. H. 1980.When is it coevolution? Evolution 34:611-612.
Johnsen, A., S. Andersson, J. Ornborg, and J. T. Lifjeld. 1998a. Ultraviolet
plumage ornamentation affects social mate choice and sperm competition
in bluethroats (Ayes: Luscinia s. svecica): a field experiment. Proc. Royal
Soc. Lond. B 265:1313-1318.
Johnsen, A., J.T. Lifjeld, P. A. Rohde, C. R. Primmer and H. Ellegren. 1998b.
Sexual conflict over fertilizations: female bluethroats escape male pater-
nity guards. Behav. Ecol. Sociobiol. 43:401-408.
Johnsen, T. S. 1998. Behavioral correlates of testosterone and seasonal
changes in steroids in red-winged blackbirds.Anim. Behav. 55: 957-965.
Johnsgard, P. A. 1994. Arena Birds. Smithsonian Inst. Press, Washington.
Johnson, K. P., F. McKinney and M. D. Sorenson. 1998. Phylogenetic con-
straint on male parental care in the dabbling ducks. Proc. Royal Soc. Lond
B 266: 759-763.
Johnston, J. P., W. J. Peach, R. D. Gregory and S. A. White. 1997. Survival
rates of temperate and tropical passerines: ATrinidadian perspective. Am.
Nat. 150: 771-789.

Jones, I. L. and F. M. Hunter. 1993. Mutual sexual selection in a monoga-
mous seabird. Nature 362: 238-239.
Jones, I. L. and F. M. Hunter. 1999. Experimental evidence for mutual inter-
and intrasexual selection favouring a crested auklet ornamentation..4nim.
Behav. 57:521-528.
Joyce, F. J. 1993. Nesting success of rufous-naped wrens (Campylorhynchus
rufinucha) is greater near wasp nests. Behav. Ecol. Sociobiol. 32:71-77.
Karr, J. R., J. D. Nichols, M. K. Klimkiewicz and J. D. Brawn. 1990. Survival
rates of birds of tropical and temperate forests: will the dogma survive?
Amer. Nat. 136:277-291.
Kempenaers, B. 1993.The uses of a breeding synchrony index. Ornis. Scand.
24: 84.
Kempenaers, B., G. R. Verheyen and A. A. Dhont. 1995. Mate guarding and
copulation behavior in monogamous and polygynous Blue Tits: do males
follow a best-of-a-bad job? Behav. Ecol. SociobioL 36: 33-42.
Kempenaers, B., G. R. Verheyen, M. Van den Broeck, T. Burke, C. Van
Broecldaoven and A. A. Dhondt. 1992. Extra-pair paternity results from
female preference for high-quality males in the blue tit. Nature 357: 494-
496.
Kennedy, R. S., P. C. Gonzales and H. C. Miranda, Jr. 1997. New Aethopyga
Sunbirds (Ayes: Nectariniidae) from the island of Mindanao, PhiUipines.
Auk 114: 1-10.
Ketterson, E. D. andV. Nolan, Jr. 1994. Parental behavior in birds. Ann. Rev.
EcoL Syst. 25:601-628.
Ketterson, E. D.,V. Nolan, Jr., L. Wolf and C. Ziegenfus. 1992. Testosterone
and avian life histories: effects of experimentally elevated testosterone on
behavior and correlates of fimess in the dark-eyed junco (Junco hyemalis).
Amer. Nat. 140: 980-999.
Klomp, H. 1970. The determination of clutch-size in birds. A review. Ardea
58:1-124.
Koenig, W. D. and F. A. Pitelka. 1981. Ecological factors and kin selection in
the evolution of cooperative breeding in birds. Pp 261-280 In: Natural
selection and social behavior (R. D. Alexander and D. W. Tinkle, Eds).
Chiron Press, NewYork.
Komdeur, J. A. 1992. Importance of habitat saturation and territory quality
for evolution of cooperative breeding in the Seychelles Warbler. Nature
358: 493--495.
Komdeur, J. A. 1996. Seasonal timing of reproduction in a tropical bird, the
Seychelles warbler: a field experiment using translocation. J. Biol. Rhythms
11: 333-350.
Komdeur, J. A., A. Huffstadt, W. Prast, G. Castle, R. Mileto and J. Wattel.
1995.Transfer experiments of SeychellesWarblers to new islands: changes
in dispersal and helping behaviour. Anita. Behav. 49: 695-708.
Konishi, M. 1969. Time resolution by single auditory neurones in birds.
Nature 222: 566-567.
REFERENCES 141
Krebs, J. R. 1982. Territorial defense in the great tit (Parus major): do resi-
dents always win? Behav. Ecol. Sociobiol. 11" 185-194.
Krebs, J. R. and N. B. Davies. 1991. Behavioral Ecology. 3rd Ed. Blackwell
Scientific Publications, Oxford.
Krebs, J. R. and D. E. Kroodsma. 1980. Repertoires and geographical varia-
tion in bird song. Adv. Stud. Behav. 11:143-177.
Krebs, J. R., R. Ashcroft and K.V. Orsdol. 1981. Song matching in the great
tit, Parus major. Anim. Behav. 29:919-923.
Kricher, J. 1997. A neotropical companion. 2nd ed. Princeton Univ. Press,
Princeton.
Krokene, C., K. Anthonisen, J.T. Lifjeld and T. Amundsen. 1996. Paternity
and paternity assurance behaviour in the bluethroat, Luscinia s. svecica.
Anim. Behav. 52:405-417.
Kroodsma, D. E.,W-C Liu, E. Goodwin and P. A. Bedell. 1999. The ecology
of song improvisation as illustrated by North American sedge wrens. Auk
116: 373-386.
Kulesza, G. 1990. An analysis of clutch-size in New World passerine birds.
Ibis 132: 407-422.
Kunkel, P. 1974. Mating systems of tropical birds: the effects of weakness or
absence of external reproduction-timing factors, with special reference to
prolonged pair bonds. Z. Tierpsychol. 34: 265-307.
Lack, D. 1947.The significance of clutch-size. Ibis 89: 302-352.
Lack, D. 1948. The significance of clutch-size. Ibis 90: 24-45.
Lack, D. 1950. The breeding seasons of European birds. Ibis 92:288-316.
Lack, D. 1954. The natural regulation of animal numbers. Clarendon Press,
Oxford.
Lack, D. 1968. Ecological adaptations for breeding in birds. Metheun, London.
Lack, D. and R. E. Moreau. 1965. Clutch-size in tropical passerine birds of
forest and savannah. Oiseau 35: 76-89.
Lambrechts, M. M., P. Perret and J. Blondel. 1996. Adaptive differences in
the timing of egg laying between different populations of birds result from
variation in photoresponsiveness. Proc. R. Soc. Lond B 163:19-22.
Langen, T. A. and S. L.Vehrencamp. 1998. Ecological factors affecting group
size and territory size in white-throated magpie-jays. Auk 115" 327-339.
Lefebvre, G., B. Poulin and R. McNeil. 1992. Settlement period and
function of long-term territory in tropical mangrove passerines. Condor
94: 83-92.
Lepson, J. K. and L. A. Freed. 1995.Variation in male plumage and behavior
of the Hawaii Akepa. Auk 112: 402-414.
Lessells, C. M. 1991 .The evolution of life histories. Pp 32-65 In: Behavioural
ecology, an evolutionary approach (J. R. Krebs and N. B. Davies, Eds). 3rd
Ed. Blackwell, Oxford.
Levey, D. J. 1988. Spatial and temporal variation in Costa Rican fruit and
fruit-eating bird abundance. Ecol. Monogr. 58:251-269.
Levey, D. J. andW. H. Karasov. 1989. Digestive responses of temperate birds
switched to fruit or insect diets. Auk 106: 675-686.
Levey, D. J. andW. H. Karasov. 1992. Digestive modulation in a seasonal fru-

givore, the American robin. Am. J. Physiol. 262:G71 l-G718.
Levey, D. J. and F. G. Stiles. 1992. Evolutionary precursors of long-distance
migration: resource availability and movement patterns in neotropical
landbirds. Am. Nat. 140: 447-476.
Levey, D. J. and F. G. Stiles. 1994. Birds: ecology, behavior and taxonomic
affinities. Pp. 217-228 In: La Selva. Ecology and natural history of a tropical
rain forest (L. A. Dade, K. S. Bawa, H. A. Hespenheide, and G. S.
Hartshorn, Eds). Chicago Univ. Press, Chicago.
Levin, R. N. 1996a. Song behaviour and reproductive strategies in a duetting
wren, Thryothorus nigricapillus. I. Removal experiments. Anim. Behav. 52:
1093-1106.
Levin, R. N. 1996b. Song behaviour and reproductive strategies in a duetting
wren, Thryothorus nigricapillus. II. Playback experiments. Anim. Behav. 52:
1107-1117.
Levin, R. N. and J. C. Wingfield. 1992. The hormonal control of territorial
aggression in tropical birds. Ornis Scand. 23:284-291.
Ligon, J. D. 1981. Demographic patterns and communal breeding in the
Green Woodhoopoe Phoeniculus purpureus. Pp 231-243 In: Natural selec-
tion and social behavior (R. D. Alexander and D. W. Tinkle, Eds). Chiron
Press, NewYork.
Ligon, J. D. and S. H. Ligon. 1990. Green woodhoopoes: life history traits
and sociality. Pp 33-65 In: Cooperative breeding in birds (P. B. Stacey andW.
D. Koenig, Eds). Cambridge Univ. Press, Cambridge.
Lill, A. 1974.The evolution of clutch size and male 'chauvinism' in the white-
bearded manakin. Living Bird 13:211-231.
Lima, S. L. 1987. Clutch size in birds: a predation perspective. Ecology 68:
1062-1070.
Lima, S. L. 1998. Stress and decision making under the risk of predation:
recent developments from behavioral, reproductive, and ecological per-
spectives. Adv. Study Behav. 27:215-290.
LoiseUe, B. A. and W. G. Hoppes. 1983. Nest predation in insular and
mainland lowland rainforest in Panama. Condor 85: 93-95.
Lovejoy, T. E., R. O. Bierregaard Jr., A. B. Rylands, J. R. Malcolm, C. E.
Quintela, L. H. Harper, K. S. Brown Jr., A. H. Powell, G.V.N. Powell, H.
O. R. Schubart and M. B. Hayes. 1986. Edge and other effects of isolation
of Amazon forest fragments. Pp 257-285 In: Conservation biology: the
science of scarcity and diversity. (M. E. Soule, Ed.). Sinauer, Sunderland,
Mass.
Lyon, B. E. and R. D. Montgomerie. 1986. Delayed plumage maturation in
passerine birds: reliable signaling by subordinate males? Evolution 40:
604-615.
Mabey, S. and E. S. Morton. 1992. Demography and territorial behavior of
wintering Kentucky warblers in Panama. Pp 329-336 In Ecology and con-
servation of neotropical migrant landbirds (J. M. Hagen and D.W. Johnston,
Eds). Smithsonian Institution Press, Washington.
REFERENCES 143
Mace, R. 1987.The dawn chorus in the great tit Parus majoris directly related
to female fertility. Nature 330: 745-746.
Macedo, R. H. and C. A. Bianchi. 1997. Communal breeding in tropical
Guira Cuckoos Guira guira: sociality in the absence of a saturated habitat.
J. Avian Biol. 28:207-215.
MacDougall-Shackleton, E. A. and R. J. Robertson. 1998. Confidence of
paternity and paternal care by eastern bluebirds. Behav. Ecol. 9:201-205.
Mader, W. J. 1982. Ecology and breeding habits of the Savannah Hawk in the
llanos of Venezuela. Condor 84:261-271.
Magrath, M. J. L. and M. A. Elgar. 1997. Paternal care declines with
increased opportunity for extra-pair matings in fairy martins. Proc. Royal
Soc. London B 264:1731-1736.
Marchant, S. 1960. The breeding of some S.W. Ecuadorian birds. Ibis 102:
349-382; 584-599.
Marler, P. 1999. On innateness: are sparrow songs 'learned' or 'innate'? Pp
293-318 In: The Design of Animal Communication (M. Hauser and M.
Konishi, Eds). M I T Press, Cambridge, Massachusetts.
Marler, P. and M. Tamura. 1962. Song 'dialects' in three populations of
white-crowned sparrows. Condor 64: 368-377.
Martin, T. E. 1987. Food as a limit on breeding birds: a life-history perspec-
tive.Ann. Rev. Ecol. Syst. 18: 453-487.
Martin, T. E. 1993. Nest predation among vegetation layers and habitat
types: revising the dogmas. Amer. Nat. 141:897-913.
Martin, T. E. 1995. Avian life history evolution in relation to nest sites, nest
predation, and food. Ecol. Monogr. 65:101-127.
Martin, T. E. 1996. Life history evolution in tropical and south temperate
birds: what do we really know? J.Avian Biol. 27: 263-272.
Martin, T. E. and A. Badyaev. 1996. Sexual dichromatism in birds: impor-
tance of nest predation and nest location for females versus males.
Evolution 50: 2454-2460.
Martin, T. E., P. R. Martin, C. R. Olson, B. J. Heidinger and J. J. Fontaine.
2000. Parental care and clutch sizes in North and South American birds.
Science 287:1482-1485.
Martinez del Rio, C. andW. H. Karasov. 1990. Digestive strategies in nectar-
and fruit-eating birds and the sugar composition of plant rewards. Am.
Nat. 136:618-656.
Matthysen, E. 1989. Territorial and nonterritorial settling in juvenile
Eurasian nuthatches (Sitta europea L.) in summer. Auk 106: 560-567.
Mauck, R. A., T. A. Waite and P. G. Parker. 1995. Monogamy in Leach's
Storm-petrel: DNA fingerprinting evidence. Auk 112: 473-482.
Maynard Smith, J. and G.A. Parker. 1976.The logic of asymmetric contests.
Anim. Behav. 24: 159-175.
McDonald, D. B. 1989. Cooperation under sexual selection: age-graded
changes in a lekking bird. Amer. Nat. 134: 709-730.
McDonald, D. B. 1993. Demographic consequences of sexual selection in
the long-tailed manakin. Behav. Ecol. 4: 297-309.
McKey, D. 1975. The ecology of coevolved seed dispersal systems. Pp

159-191 In: Coevolution of animals and plants (L. E. Gilbert and P. R.
Raven, Eds). University of Texas Press, Austin.
McKinney, F. 1985. Primary and secondary male reproductive strategies of
dabbling ducks. Pp 68-82 In: Avian Monogamy (P. A. Gowaty and D.W.
Mock, Eds). Ornithol. Monogr. 37, American Ornithologists Union, Wash-
ington DC.
McKinney, F. and G. Brewer. 1989. Parental attendance and brood care in
four Argentine dabbling ducks. Condor 91:131-138.
McKinney, F., S. R. Derrickson and P. Mineau. 1983. Forced copulation in
waterfowl. Behaviour 86: 250-294.
Medsger, O. P. 1931. Nature rambles. Spring. Corwall Press, NewYork.
Melland, R. R. 2000. The genetic mating system and population structure of
the Green-rumped Parrotlet. PhD Dissertation, Univ. of North Dakota,
Grand Forks, ND.
Midgley, J. J. and W. J. Bond. 1991. Ecological aspects of the rise of
angiosperms: a challenge to the reproductive superiority hypothesis. Biol.
J. Linn. Soc. 44:81-92.
Miller, A. H. 1962. Bimodal occurrence of breeding in an equatorial sparrow.
Proc. Natl.Acad. Sci. 48: 396-400.
Moermond, T. C. and J. S. Denslow. 1985. Neotropical avian frugivores:
Patterns of behavior, morphology, and nutrition with consequences for
fruit selection. Pp 867-897 In: Neotropical ornithology (P. A. Buckley, M. S.
Foster, E. S. Morton, R. S. Ridgely and F. G. Buckley, Eds). Ornith.
Monog. 36, Allen Press, Lawrence.
Moiler, A. P. 1988. Female choice selects for male sexual tail ornaments.
Nature 332: 640-642.
Moiler, A. P. 1991. Why mated songbirds sing so much: mate guarding and
male announcement of mate fertility status. Amer. Nat. 138:994-1014.
Moiler, A. P. 1992. Sexual selection in the monogamous swallow Hirundo
rustica. II. Mechanisms of intersexual selection. J. Evol. Biol. 5: 603-624.
Moiler, A. P. 1994. Sexual selection and the barn swallow. Oxford Univ. Press,
Oxford.
Moiler, A. P. 1997. Immunce defence, extra-pair paternity, and sexual selec-
tion in birds. Proc. R. Soc. Lond. B 264:561-566.
Moiler, A. P. and T. R. Birkhead. 1994. The evolution of plumage brightness
in birds is related to extra-pair paternity. Evolution 48:1089-1100.
Moiler, A. P. and J.V. Briskie. 1995. Extrapair paternity, sperm competition
and the evolution of testis size in birds. Behav. Ecol. Sociobiol. 36: 357-365.
Moiler, A. P., R. Dufva and J. Erritzoe. 1998a. Host immune function and
sexual selection in birds. J. Evol. Biol. 11:703-719.
Moiler, A. P., P.-Y. Henry and J. Erritzoe. 2000. The evolution of song reper-
toires and immune defense in birds. Proc. Biol. Soc. Lond. 267:1439.
Moore, O., B. J. M. Stutchbury and J. Quinn. 1999. Extra-pair mating system
of an asynchronously breeding tropical songbird, the Mangrove Swallow.
Auk 116: 1039-1046.
REFERENCES 145
Moreau, R. E. 1937. Breeding seasons of birds in East African evergreen

forest. Proc. Zool. Soc. Lond. 136:631-653.
Moreau, R. E. 1950.The breeding seasons of African birds. 1. Land birds. Ibis
92: 223-267.
Morse, D. H. 1970. Ecological aspects of some mixed-species flocks of birds.
Ecol. Monogr. 40:119-168.
Morse, D. H. 1974. Niche breadth as a function of social dominance. Am.
Nat. 108:818-830.
Morse, D. H. 1977. Feeding behavior and predator avoidance in heterospe-
cific groups. BioScience 27: 332-339.
Morton, E. S. 1968. Robins feeding on hairy caterpillars. Auk 85: 696.
Morton, E. S. 1971 a. Food and migration habits of the eastern kingbird in
Panama. Auk 88: 925-926.
Morton, E. S. 197 lb. Nest predation affecting the breeding season of the
clay-colored robin, a tropical song bird. Science 181:920-921.
Morton, E. S. 1973. On the evolutionary advantages and disadvantages of
fruit eating in tropical birds.Amer. Nat. 107: 8-22.
Morton, E. S. 1977a. Intratropical migration in the yellow-green vireo and
piratic flycatcher. Auk 94: 97-106.
Morton, E. S. 1977b. On the occurrence and significance of motivation-
structural rules in some bird and mammal sounds. ,4mer. Nat. 111:
855-869.
Morton, E. S. 1978. Reintroducing recently extirpated birds into a tropical
forest preserve. Pp 379-384 In: Endangered birds: management techniquesfor
preserving threatened species (S. A. Temple, Ed.). Univ. of Wisconsin Press,
Madison.
Morton, E. S. 1979a. A comparative survey of avian social systems in
northern Venezuelan habitats. Pp 233-259 In: Vertebrate ecology in the
northern neotropics (J. F. Eisenberg, Ed.). Smithsonian Institution Press,
Washington.
Morton E. S. 1979b. Effective pollination of Erythrina fusca by the Orchard
Oriole (Icterus spurius) : coevolved behavioral manipulation? Ann. Missouri
Bot. Garden 66: 482-489.
Morton, E. S. 1980. Adaptations to seasonal changes by migrant land birds
in the Panama Canal Zone. Pp 437-453 In: Migrant birds in the neotropics:
ecology, behavior, distribution, and conservation (A. Keast and E. S. Morton,
Eds). Smithsonian Institution Press, Washington.
Morton, E. S. 1982. Grading, discreteness, redundancy, and motivation-
structural rules. Pp 183-212 In: Acoustic communication in birds, vol. 1 (D.
E. Kroodsma and T. E. Miller, Eds). Academic Press, NewYork.
Morton, E. S. 1983. Turdus grayi. Pp 610-611 In: Costa Rican Natural
History (D. J. Janzen, Ed.). Univ. of Chicago Press, Chicago.
Morton, E. S. 1986. Predictions from the ranging hypothesis for the evolu-
tion of long distance signals in birds. Behaviour 99: 65-86.
Morton, E. S. 1987. The effects of distance and isolation on song-type
sharing in the CarolinaWren. Wilson Bull. 99:601-610.
Morton, E. S. 1992.What do we know about the future of migrant landbirds?

Pp. 579-589 In: Ecology and conservation of neotropical landbirds (J. M.
Hagen and D.W. Johnston, Eds). Smithsonian Institution Press,Washing-
ton.
Morton, E. S. 1996a.Why songbirds learn songs: an arms race over ranging?
Poultry and Avian Biology Reviews 7:65-71.
Morton, E. S. 1996b. A comparison of vocal behavior among tropical and
temperate passerine birds. Pp 258-268 In: Ecology and evolution of acoustic
communication in birds (D. E. Kroodsma and E. H. Miller, Eds). Cornell
Univ. Press, Ithaca.
Morton, E. S. and K. C. Derrickson. 1996. Song ranging by the dusky
antbird, Cercomacra tyrannina: ranging without song learning. Behav. Ecol.
Sociobiol. 39:195-201.
Morton, E. S. and J. Page. 1992. Animal Talk: science and the voices of nature.
Random House, NewYork.
Morton, E. S. and M. D. Shalter. 1977. Vocal response to predators in pair-
bonded Carolina Wrens. Condor 79: 222-227.
Morton E. S. and B. J. M. Stutchbury. 2000. Demography and reproductive
success in the dusky antbird, a sedentary tropical passerine. J. Field
Ornithol. 71: 493-500.
Morton, E. S., G. Geitgey, and S. McGrath. 1978. On bluebird 'responses to
apparent female adultery.' Amer. Nat. 112:968-971.
Morton E. S., J. Lynch, K. Young and P. Mehlhop. 1986. Do male Hooded
Warblers exclude females from nonbreeding territories in tropical forests?
Auk 104: 133-135.
Morton, E. S., L. Forman and M. Braun. 1990. Extra-pair fertilizations and
the evolution of colonial breeding in purple martins.Auk 107: 275-283.
Morton, E. S., B. J. M. Stutchbury, J. S. Howlett and W. H. Piper. 1998.
Genetic monogamy in blue-headed vireos and a comparison with a sym-
patric vireo with extrapair paternity. Behav. Ecol. 9:515-524.
Morton, E. S., K. C. Derrickson and B. J. M. Stutchbury. 2000. Territory
switching in a sedentary tropical passerine the dusky antbird Cercomacra
tyrannina. Behav. Ecol., in press.
Moynihan, M. 1962.The organization and probable evolution of some mixed
species flocks of Neotropical birds. Srnithsonian Misc. Coll. 143:1-140.
Moynihan, M. 1998. The social regulation of competition and aggression: with a
discussion of tactics and strategies. Smithsonian Inst. Press, Washington.
Munn, C. A. 1985. Permanent canopy and understory flocks in Amazonia:
species composition and population density. Pp 683-712. In: Neotropical
ornithology (P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely and R.
G. Buckley, Eds). Ornithological Monograph 36. Allen Press, Kansas.
Munn, C.A. 1986. Birds that 'cry wolf'. Nature 319:143-145.
Munn, C.A. and J.W.Terborgh. 1979. Multi-species territoriality in neotrop-
ical foraging flocks. Condor 81: 338-347.
Murray, B. G., Jr. 1985. Evolution of clutch size in tropical species of birds.
Ornithol. Monogr. 36:505-519.
REFERENCES 147
Murray, K. G., S. Russell, C. M. Picone, K. Winnett-Murray, W. Sherwood

and M. L. Kuhlmann. 1994. Fruit laxatives and seed passage rates in
frugivores: consequences for plant reproductive success. Ecology 75:
989-994.
Naef-Daenzer, B. and L. F. Keller. 1999. The foraging performance of great
and blue tits (Parus major and R caeruleus) in relation to caterpillar devel-
opment, and its consequences for nestling growth and fledgling weight. J.
Anim. Ecol. 68:708-718.
Nager, R. G. and A. J. van Noordwijk. 1995. Proximate and ultimate aspects
of phenotypic plasticity in timing of great tit breeding in a heterogenous
environment. Amer. Nat. 146: 454-474.
Naguib, M. 1995. Auditory distance assessment of singing conspecifics in
Carolina wrens: the role of reverberation and frequency-dependent atten-
uation. Anim. Behav. 50:1297-1307.
Nealen, P. M. and D. J. Perkel. 2000. Sexual dimorphism in the song system
of the Carolina wren Thryothorus ludovicianus. J. Comp. Neurol. 418:
346-360.
Nee, S. and R. M. May. 1997. Extinction and the loss of evolutionary history.
Science 278: 692-694.
Negro, J. J., M. Villarroel, J. L. TeUa, U. Kuhnleiu, E Hilaldo, J. A. Donazar
and D. M. Bird. 1996. DNA fingerprinting reveals low incidence of EPFs
in the Lesser Kestrel.Anim. Behav. 51: 935-943.
Neudorf, D. L., B. J. M. Stutchbury and W. H. Piper. 1997. Covert extrater-
ritorial behavior of female hooded warblers. Behav. Ecol. 8: 595-600.
Nice, M. M. 1937. Studies in the life history of the Song Sparrow-I. Trans.
Linn. Soc. N.Y. 4: 1-247.
Nilsson, J. A. and E. Svensson. 1993. Energy constraints and ultimate deci-
sions during egg-laying in the blue tit. Ecology 74:244-251.
Norris, D. R. and B. J. M. Stutchbury. 2001. Extra-territorial movements of
a forest songbird in a fragmented landscape. Cons. Biol. in press.
Nowicki, S., S. Peters and J. Podos. 1998. Song learning, early nutrition, and
sexual selection in songbirds. Amer. Zool. 38:179-190.
Nur, N. 1988. The consequences of brood size for breeding blue tits. III.
Measuring the cost of reproduction: survival, future fecundity, and differ-
ential dispersal. Evolution 42:351-362.
Nur, N. 1990. The cost of reproduction in birds: evaluating the evidence
from manipulative and non-manipulative studes. Pp 281-296 In: Popula-
tion biology ofpasserine birds, an integrated approach (J. Blondel, A. Gosler, J.
D. Lebreton and R. McCleery, Eds). Springer-Verlag.
Ohala, J. J. 1984. An ethological perspective on common cross-language uti-
lization ofF0 of voice. Phonetica 41:1-16.
Oniki, Y. 1979. Is nesting success of birds low in the Tropics? Biotropica 11"
60-69.
Orians, G. H. 1969. On the evolution of mating systems in birds and
mammals. Amer. Nat. 103: 589-603.
Orians, G. H. 1985. Blackbirds of the Americas. Univ. of Washington Press,
Seattle.
Oring, L. W., A. J. Fivizzani and M. E. E1 Halawani. 1989. Testosterone-
induced inhibition of incubation in the spotted sandpiper (Actitis
mecularia). Horm. Behav. 23:412-423.
Otter, K., L. Ratcliffe and P. T. Boag. 1994. Extra-pair paternity in the
Black-capped Chickadee. Condor96:218-222.
Otter, K., B. Chruszcz and L. Ratcliffe. 1997. Honest advertisement and
song output during the dawn chorus of black-capped chickadees. Behav.
Ecol. 8:167-173.
Otter, K., L. Ratcliffe, D. Michaud and P.T. Boag. 1998. Do female black-
capped chickadees prefer high-ranking males as extra-pair partners?
Behav. Ecol. Sociobiol. 43: 25-36.
Owings, D. H. and E. S. Morton. 1998. Animal vocal communication: a new
approach. Cambridge Univ. Press, Cambridge.
Park, S. R. and D. Park. 2000. Song type for intrasexual interaction in the
bush warbler.Auk 117: 228-232.
Parrish, J. D. 2000. Behavioral, energetic, and conservation implications of
foraging plasticity during migration. Studies in Avian Biol. 20: 53-70.
P~rt, T. 1991. Is dawn singing related to paternity insurance? The case of the
collared flycatcher. Anim. Behav. 41:451-456.
Payne, R. B. 1983. The social context of song mimicry: song matching
dialects in Indigo Buntings (Passerina cyanea).Anim. Behav. 31: 788-805.
Payne, R. B. 1996. Song traditions in indigo buntings: origin, improvisation,
dispersal, and extinction in cultural evolution. Pp 198-221 In: Ecology and
evolution of acoustic communication in birds (D. E. Kroodsma and E. H.
Miller, Eds). Cornell University Press, Ithaca.
Peek, F.W. 1972. An experimental study of the territorial function of vocal
and visual displays in the male red-winged blackbirds (Agelaius
phoeniceus). Anim. Behav. 29:112-178.
Perrins, C. M. 1970. The timing of birds' breeding seasons. Ibis 112:
242-255.
Perrins, C. M. 1991. Tits and their caterpillar food supply. Ibis 133: 49-54.
Peters, W. D. and T. C. Grubb, Jr. 1983. An experimental analysis of sex-
specific foraging in the DownyWoodpecker, Picoides pubescens. Ecology 64:
1437-1443.
Petren, K., B. R. Grant and P. R. Grant. 1999. Low extrapair paternity in the
Cactus Finch (Geospiza scandens).Auk 116: 252-256.
Pitcher, T. E. and B. J. M. Stutchbury. 2000. Extraterritorial forays and male
parental care in hooded warblers. Anita. Behav. 59:1261-1269.
Poulin, B., G. Lefebvre and R. McNeil. 1992. Tropical avian phenology in
relation to abundance and expoitation of food resources. Ecology 73:
2295-2309.
Poulin, R. 1996. Sexual inequalities in helminth infections: a cost of being
male? Amer. Nat. 147: 287-295.
Powell, G.V.N. 1979. Structure and dynamics of interspecific flocks in a
Neotropical mid-elevation forest. Auk 96: 375-390.
REFERENCES 149
Powell, G.V.N. 1985. Sociobiology and adaptive significance ofinterspecific

foraging flocks in the neotropics. Pp 713-732 In: Neotropical ornithology
(P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely and R. G.
Buckley, Eds). Ornithological Monograph 36. Allen Press, Kansas.
Prum, R. O. andV. R. Razafindratsita. 1997. Lek behavior and natural history
of the Velvet Asite (Philepitta castanea: Eurylaimidae). Wilson Bull. 109:
371-392.
Purvis, A., P-M Agapow, J. L. Gittleman and G. M. Mace. 2000. Nonrandom
extinction and the loss of evolutionary history. Science 288: 328-330.
Quarstr6m, A. 1997. Experimentally increased badge size increases male
competition and reduces male parental care in the collared flycatcher.
Proc. Royal Soc. Lond. B 264:1225-1231.
Quinn, J. S., G. E. Woolfenden, J. W. Fitzpatrick and B. N. White. 1999.
Multi-locus fingerprinting supports monogamy in Florida scrub-jays.
Rabenold, K. N. 1990. Campylorhynchus wrens: the ecology of delayed dis-
persal and cooperation in the Venezuelan savannah. Pp 157-196 In:
Cooperative breeding in birds: long term studies of ecology and behavior (P. B.
Stacey andW. D. Koenig, Eds). Cambridge Univ. Press, Cambridge.
Rabenold, E P., K. N. Rabenold, W. H. Piper and S.W. Zack. 1990. Shared
paternity revealed by genetic analysis in cooperatively breeding tropical
wrens. Nature 348: 538-540.
Rabol, J. 1987. Coexistence and competition between overwintering Willow
Warblers Phylloscopus trochilus and local warblers at Lake Naivasha,
Kenya. Ornis Scand. 18:101-121.
Radesater, T., S. Jakobsson, N. Andbjer, A. Bylin and K. Nystrom. 1987.
Song rate and pair formation in the willow warbler, Phylloscopus trochilus.
Anita. Behav. 35:1645-1651.
Ralph, C. J. and S. G. Fancy. 1994. Timing of breeding and molting in six
species of Hawaiian honeycreepers. Condor 96:151-161.
Ramsay, S. L. and D. C. Houston. 1997. Nutritional constraints on egg pro-
duction in the blue tit: a supplementary feeding study..7. Anim. Ecol. 66:
649-657.
Raouf, S. A., P. G. Parker, E. D. Ketterson, V. Nolan Jr., and C. Ziegenfus.
1997. Testosterone affects reproductive success by influencing extra-pair
fertilizations in male dark-eyed juncos (Aves:Junco hyemalis). Proc. R. Soc.
Lond. B 264:1599-1603.
Rappole, J. H. 1995. The ecology of migrant birds, a Neotropical perspective.
Smithsonian Inst. Press, Washington, D. C.
Rappole, J. H. and E. S. Morton. 1985. Effects of habitat alteration on a
tropical avian forest community. Pp 1013-1021 In: Neotropical ornithology
(Buckley, P. A., M. S. Foster, E. S. Morton, R. S. Ridgely and R. G.
Buckley, Eds). Ornithological Monograph 36. Allen Press, Kansas.
Rappole, J. H., E. S. Morton, T. E. Lovejoy III, and J. L. Ruos. 1983. Nearctic
avian migrants in the Neotropics. USDI, Fish andWildlife Service,Washing-
ton, D. C. 384 pp.
Ratcliffe, L. and K. Otter. 1996. Sex differences in song recognition. Pp

339-355 In: Ecology and evolution of acoustic communication in birds (D. E.
Kroodsma and E. H. Miller, Eds). Cornell Univ. Press, Ithaca.
Regal, P. J. 1976. Ecology and evolution of flowering plant dominance.
Science 196: 622-629.
Reid, M. L. 1987. Costliness and reliability in the singing vigour of Ipswich
sparrow. Anim. Behav. 35:1735-1743.
Remsen, J. V., Jr. 1984. High incidence of 'leapfrog' pattern of geographic
variation in Andean birds: implications for the speciation process. Science
224:171-172.
Restrepo, C. and M. L. Mondrag6n. 1998. Cooperative breeding in the fru-
givorous Toucan Barbet (Semnornis ramphastinus). Auk 115: 4-15.
Reyer, H. U. 1990. Pied Kingfishers: ecological causes and reproductive con-
sequences of cooperative breeding. Pp 527-558 In: Cooperative breeding in
birds: long term studies of ecology and behavior (P. B. Stacey and W. D.
Koenig, Eds). Cambridge Univ. Press, Cambridge.
Richards, D. G. 1981. Estimation of distance of singing conspecifics by the
Carolina wren.Auk 98: 127-133.
Richardson, K. C. and R. D.Wooller. 1988.The alimentary tract of a special-
ist frugivore, the mistletoebird, Dicaeum hirundinaceum, in relation to its
diet. Australian J. Zool. 36: 373-382.
Ricklefs, R. 1966. The temporal component of diversity among species of
birds. Evolution 20: 235-242.
Ricklefs, R. E. 1969a. An analysis of nesting mortality in birds. Smithsonian
Contr. Zool. 9: 1-48.
Ricklefs, R. 1969b. The nesting cycle of songbirds in tropical and temperate
regions. Living Bird 8: 1-48.
Ricklefs, R. E. 1977. On the evolution of reproductive strategies in birds:
reproductive effort. Amer. Nat. 111: 453-478.
Ricklefs, R. E. 1980. Geographical variation in clutch size among passerine
birds: Ashmole's hypothesis. Auk 97: 38-49.
Ricklefs, R. 1997. Comparative demography of New World populations of
thrushes (Turdus spp.). Ecol. Monogr. 67: 23-43.
Ridgely, R. S. and J. A. Gwynne. 1989. A guide to the birds of Panama. 2nd ed.
Princeton Univ. Press, Princeton.
Ritchison, G. 1983. The function of singing in female black-headed gros-
beaks: family-group maintenance. Auk 100:105-116.
Robbins, M. B., G. H. Rosenberg and F. S. Molina. 1994. A new species of
cotinga (Cotingidae: Doliornis) from the Ecuadorian Andes, with
comments on plumage sequences in Doliornis and Ampelion.Auk 111: 1-7.
Robertson, B. C. 1996. The mating system of the Capricorn silvereye. Ph.D.
Dissertation. University of Queensland, St. Lucia, Brisbane.
Robinson, D. 1990. The nesting ecology of sympatric Scarlet Robin Petroica
multicolor and Flame Robin P. phoenicea populations in open Eucalypt
forest. Emu 90:40-52.
Robinson, S. K. 1985. Coloniality in the yellow-rumped cacique as a defense
REFERENCES 151
against nest predators. Auk 102:506-519.

Robinson, S. K. 1986. Competitive and mutualistic interactions among
females in a neotropical oriole. Anim. Behav. 34:113-122.
Robinson, S. K. and J. Terborgh. 1995. Interspecific aggression and habitat
selection by Amazonian birds. J. Anim. Ecol. 64:1-11.
Robinson, S. K., F. R.Thompson III, T. M. Donovan, D. R.Whitehead and J.
Faaborg. 1995. Regional forest fragmentation and the nesting success of
migratory birds. Science 267:1987-1990.
Robinson, T. R.,W. D. Robinson and E. C. Edwards. 2000. Breeding ecology
and nest-site selection of Song Wrens in central Panama. Auk 117:
345-354.
Robinson, W. D., T. R. Robinson, S. K. Robinson and J. D. Brawn. 2000.
Nesting success ofunderstory forest birds in central Panama.J.Avian Biol.
31: 151-164.
Rohwer, S. 1982. The evolution of reliable and unreliable badges of fighting
ability. Amer. Zool. 22:531-546.
Rohwer, S. and G. S. Butcher. 1988. Winter versus summer explanations of
delayed plumage maturation in passerine birds.Amer. Nat. 131: 556-572.
Rohwer, S. and E. Roskaft. 1989. Results of dyeing male yellow-headed
blackbirds solid black: implications for the arbitrary identity badge
hypothesis. Behav. Ecol. Sociobiol. 25: 39-48.
Rohwer, S., S. D. Fretwell and D. M. Niles. 1980. Delayed maturation in
passerine plumages and the deceptive acquistion of resources. Amer. Nat.
115: 400-437.
Roper, J. J. and R. R. Goldstein. 1997. A test of the Skutch hypothesis: does
activity at nests increase nest predation risk? J. Avian Biol. 28:111-117.
Rowan, M. K. 1966. Territory as a density-regulating mechanism in some
South African birds. Ostrich (suppl.) 6: 397-408.
Rowley, I. and E. Russell. 1991. Demography of passerines in the temperate
southern hemisphere. Pp 22-44 In: Bird population studies: relevance to con-
servation, demography and management (C. M. Perrins, J. D. Lebreton and
G. J. M. Hirons, Eds). Oxford Univ. Press, Oxford.
Saino, N., A. M. Bolzern and A. P. Moller. 1997a. Immunocompetence,
ornamentation, and viability of male barn swallows (Hirundo rustica).
Proc. Natl.Acad. Sci. USA 94: 549-552.
Saino, N., C. R. Primmer, H. Ellegren and A. P. Moller. 1997b. An experi-
mental study of paternity and tail ornamentation in the barn swallow
(Hirundo rustica). Evolution 51:562-570.
Sandercock, B. K., S. R. Beissinger, S. H. Stoleson, R. R. Melland and C. R.
Hughes. 2000. Survival rates of a neotropical parrot: implications for lati-
tudinal comparisons of avian demography. Ecology 81: 1351-1370.
Sargent, S. 1993. Nesting biology of the Yellow-throated Euphonia: large
clutch size in a neotropical frugivore. Wilson Bull. 105: 285-300.
Schneider, K.J. 1984. Dominance, predation, and optimal foraging inWhite-
throated Sparrow flocks. Ecology 65:1820-1827.
Schoech, S.J. 1996. The effect of supplemental food on body condition and
the timing of reproduction in a cooperative breeder, the Florida scrub jay.

Condor 98: 234-244.
Schwagmeyer, P. L. and E. D. Ketterson. 1999. Breeding synchrony and EPF
rates: the key to a can of worms? Trends Ecol. Evol. 14: 47-48.
Schwagmeyer, P. L., R. C. St. Clair, J. D. Moodie, T. C. Lamey, G. D. Schnell
and M. N. Moodie. 1999. Species differences in male parental care in
birds: a reexamination of correlates with paternity. Auk 116: 487-503.
Sealy, S. G. 1989. Defence of nectar sources by migrating Cape May
Warblers. J. Field Ornithol. 60: 89-93.
Searcy, W. A. and K.Yasukawa. 1996. Song and female choice. Pp 454-473
In: Ecology and evolution of acoustic communication in birds (D. E.
Kroodsma, and E. H. Miller, Eds). Cornell Univ. Press, Ithaca.
Selander, R. K. 1965. On mating systems and sexual selection.Amer. Nat. 99:
129-141.
Sheldon, B. C. 1994. Sperm competition in the chaffinch: the role of the
female. Anim. Behav. 47:163-173.
Sick, H. 1993. Birds in Brazil. Princeton U. Press.
Sieving, K. E. 1992. Nest predation and differential insular extinction among
selected forest birds of central Panama. Ecology 73:2310-2328.
Simmons, R. E. 1993. Effects of supplementary food on density-reduced
breeding in an African eagle: adaptive restraint or ecological constraint?
Ibis 135: 394-402.
Sinclair, A. R. E. 1978. Factors affecting the food supply and breeding season
of resident birds and movements of Palearctic migrants in a tropical
African savannah. Ibis 120: 480-497.
Skutch, A. F. 1935. Helpers at the nest. Auk 52: 257-273.
Skutch, A. E 1949. Do tropical birds rear as many young as they can nourish?
Ibis 91: 430-455.
Skutch, A. F. 1950.The nesting seasons of Central American birds in relation
to climate and food supply. Ibis 92:185-222.
Skutch, A. F. 1954. Life Histories of Central American Birds. Pacific Coast
Avifauna No. 31, Cooper Ornithological Society, Berkeley California.
Skutch, A. F. 1960. Life histories of Central American birds. Pacific Coast
Avifauna 34: 1-593.
Skutch, A. F. 1969. Life histories of Central American birds. Pacific Coast
Avifauna 35: 1-580.
Skutch, A. F. 1981. New studies of tropical American birds. Publ. Nuttall
Ornithol. Club No. 19.
Skutch, A. E 1985. Clutch size, nesting success, and predation on nests of
neotropical birds, reviewed. Ornithol. Monogr. 36: 575-594.
Skutch, A. F. 1996. Antbirds and ovenbirds. Univ. of Texas Press, Austin.
Skutch, A. F. 1997. Life ofthe Flycatcher. Univ. of Oklahoma Press, Oklahoma.
Slagsvold, T. and J. Lifjeld. 1997. Incomplete female knowledge may explain
variation in extra-pair paternity in birds. Behavior 134:1-19.
Smith, D. G. 1972. The role of the epaulets in the Red-winged Blackbird
social system (Agelaius phoeniceus). Behavior 41:251-268.
REFERENCES 153
Smith, S. M. 1978. The 'underworld' in a territorial sparrow: adaptive

strategy for floaters. Amer. Nat. 112:571-582.
Smith, S. M. 1988. Extra-pair copulations in Black-capped Chickadees: the
role of the female. Behaviour 107:15-23.
Smith, S. M. 1991. The Black-capped Chickadee. Cornell University Press,
Ithaca.
Snow, B. K. 1970. A field study of the bearded bellbird in Trinidad. Ibis 112:
299-329.
Snow, B. K. 1974. Lek behaviour and breeding of Guy's Hermit Humming-
bird Phaethornis guy. Ibis 116: 278-297.
Snow, B. K. and D.W. Snow. 1979. The Ochre-bellied Flycatcher and the
evolution oflek behavior. Condor 81" 286-292.
Snow, B. K. and D.W. Snow. 1988. Birds and Berries. T & A D Poyser, Calton.
Snow, D.W. 1962. A field study of the Black and White Manakin, Manacus
manacus, in Trinidad. Zoologica 47" 65-104.
Snow, D.W. 1965. A possible selective factor in the evolution of fruiting
seasons in tropical forest. Oikos 15:274-281.
Snow, D.W. 1971. Evolutionary aspects of fruit-eating by birds. Ibis 113:
194-202.
Snow, D.W. 1976a. The relationship between climate and annual cycles in
the Cotingidae. Ibis 118:366-401.
Snow, D.W. 1981. Tropical frugivorous birds and their food plants: a world
survey. Biotropica 13:1-14.
Snow, D.W. and A. Lill. 1974. Longevity records for some Neotropical land-
birds. Condor 76: 262-267.
Snow, D.W. and B. K. Snow. 1963. Breeding and the annual cycle in three
Trinidad thrushes. Wilson Bull. 75: 27-41.
Snow, D.W. and B. K. Snow. 1973.The breeding ofthe Hairy Hermit Glaucis
hirsuta in Trinidad. Ardea 61:106-122.
Soler, M., M. Martin-Vivaldi, J. M. Marin and A. P. Moiler. 1999. Weight
lifting and health status in the black wheatear. Behav. Ecol. 10:281-286.
Sorenson, L. G. 1992. Variable mating system of a sedentary tropical duck:
the White-cheeked Pintail (Anas bahamensis bahamensis). Auk 109:
277-292.
Stacey, P. B. and J. D. Ligon. 1991. The benefits-of-philopatry hypothesis for
the evolution of cooperative breeding: variation in territory quality and
group size effects. Amer. Nat. 137:831-846.
Staicer, C. A. 1992. Social behavior of the Northern Parula, Cape May
Warbler, and Prairie Warbler wintering in second-growth forest in south-
western Puerto Rico. Pp 309-320 In: Ecology and conservation ofneotropical
migrant landbirds (J. M. Hagan III and D.W. Johnston, Eds). Smithsonian
Inst. Press, Washington.
Staicer, C. A., D. A. Spector and A. G. Horn. 1996. The dawn chorus and
other diel patterns in acoustic signaling. Pp 426-453 In: Ecology and evo-
lution of acoustic communication in birds (D. E. Kroodsma and E. H. Miller,
Eds). Cornell Univ. Press, Ithaca.
Stiles, E.W. 1980. Patterns of fruit presentation and seed dispersal in bird-
disseminated woody plants in the eastern deciduous forest. Amen Nat.
116: 670-688.
Stiles, F. G. 1980. The annual cycle in a tropical wet forest hummingbird
community. Ibis 122: 322-343.
Stiles, F. G. 1992. Effects of a severe drought on the population biology of a
tropical hummingbird. Ecology 73:1375-1390.
Stiles, F. G. and L. L. Wolf. 1974. A possible circannual molt rhythm in a
tropical hummingbird.Amer. Nat. 108: 341-354.
Stiles, F. G. and L. L. Wolf. 1979. Ecology and evolution of lek mating
behavior in the long-tailed hermit hummingbird. Ornithol. Monogr. 27.
American Ornithol. Union.
Stokes, A.W. 1974. Territory. Benchmark papers in animal behavior. Dowden,
Hutchinson & Ross, Inc., Stroudsburg, PA.
Stoleson, S. H. and S. R. Beissinger. 1997. Hatching asynchrony, brood
reduction, and food limitation in a neotropical parrot. Ecol. Monogr. 67:
131-154.
Stouffer, P. C. 1997. Interspecific aggression in Formicarius antthrushes?The
view from central Amazonian Brazil. Auk 114: 780-785.
Strahl, S. D. and A. Schmitz. 1990. Hoatzins: cooperative breeding in a foliv-
orous neotropical bird. Pp 131-156 In: Cooperative breeding in birds: long
term studies of ecology and behavior (P. B. Stacey and W. D. Koenig, Eds).
Cambridge Univ. Press, Cambridge.
Strain, J. G. and R. L. Mumme. 1988. Effects of food supplementation, song
playback, and temperature on vocal territorial behavior of Carolina
Wrens. Auk 105:11-16.
Stratford, J. A. and P. C. Stouffer. 1999. Local extinctions of terrestrial insec-
tivorous birds in a fragmented landscape near Manaus, Brazil. Cons. Biol.
13: 1416-1423.
Studd, M.V. and R. J. Robertson. 1985. Life span, competition, and delayed
plumage maturation in male passerines: the breeding threshold hypothe-
sis. Amer. Nat. 126:101-115.
Stutchbury, B. J. 1991. The adaptive significance of male subadult plumage
in purple martins: plumage dyeing experiments. Behav. Ecol. Sociobiol. 29:
297-306.
Stutchbury, B. J. 1992. Experimental evidence that bright coloration is not
important for territory defense in purple martins. Behav. Ecol. Sociobiol.
31: 27-33.
Stutchbury, B.J. 1994. Competition for winter territories in a Neotropical
migrant songbird: the role of age, sex, and color. Auk 111: 63-69.
Stutchbury, B. J. M. 1998a. Female mate choice of extra-pair males: breeding
synchrony is important. Behav. Ecol. Sociobiol. 43:213-215.
Stutchbury, B. J. M. 1998b. Extra-pair mating effort of male hooded
warblers, Wilsonia citrina.Anim. Behav. 55:553-561.
Stutchbury, B. J. M. and J. S. Howlett. 1995. Does male-like coloration in
female Hooded Warblers increase nest predation? Condor 97: 559-564.
REFERENCES 155
Stutchbury, B. J. and E. S. Morton. 1995. The effect of breeding synchrony

on extra-pair mating systems in songbirds. Behaviour 132: 675-690.
Stutchbury, B. J. M. and D. Neudorf. 1998. Female control, breeding syn-
chrony and the evolution of extra-pair mating strategies. Pp 103-122 In:
Avian reproductive tactics: female and male perspectives, (P. Parker and
N. Burley, Eds.). Ornithol. Monogr. 49, Amer. Ornithol. Union.
Stutchbury, B. J. and R. J. Robertson. 1987a. Behavioral tactics of subadult
female floaters in the tree swallow. Behav. Ecol. Sociobiol. 20:413-419.
Stutchbury, B. J. and R. J. Robertson. 1987b. Signaling subordinate and
female status: two hypotheses for the adaptive significance of subadult
plumage in female tree swallows.Auk 104:717-723.
Stutchbury, B. J., J. M. Rhymer, and E. S. Morton. 1994. Extra-pair paternity
in the hooded warbler. Behav. Ecol. 5: 384-392.
Stutchbury, B. J. M., W. H. Piper, D. L. Neudorf, S. A. Tarof, J. M. Rhymer,
G. Fuller and R. C. Fleischer. 1997. Correlates of extra-pair fertilization
success in hooded warblers. Behav. Ecol. Sociobiol. 40:119-126.
Stutchbury, B. J. M., E. S. Morton and W. H. Piper. 1998. Extra-pair mating
system of a synchronously breeding tropical songbird. J. Avian Biol. 29:
72-78.
Sullivan, K.A. 1984.The advantages of social foraging in DownyWoodpeck-
ers. Anita. Behav. 32:16-22.
Svensson, E. 1997. Natural selection on avian breeding time: causality,
fecundity-dependent, and fecundity-independent selection. Evolution 51:
1276-1283.
Svensson, E. and J. A. Nilsson. 1995. Food supply, territory quality, and
reproductive timing in the blue tit (Parus caeruleus). Ecology 76:
1804-1812.
Tallman, D. A. and E. J. Tallman. 1997. Timing of breeding by antbirds
(Formicariidae) in an aseasonal environment in Amazonian Ecuador.
Ornithol. Monogr. 48: 783-789.
Tarburton, M. K. 1987. An experimental manipulation of clutch and brood
size of white-rumped swiftlets Aerodramus spodiopygius of Fiji. Ibis 129:
107-114.
Tarof, S. A., B. J. M. Stutchbury, W. H. Piper and R. C. Fleischer. 1998. Does
high breeding density increase the frequency of extra-pair fertilizations in
HoodedWarblers? J.Avian Biol. 29:145-154.
Temeles, E. J., I. L. Pan, J. L. Brennan and J. N. Horwitt. 2000. Evidence for
ecological causation of sexual dimorphism in a hummingbird. Science 289:
441-443.
Terborgh J. 1990. Mixed flocks and polyspecific associations: costs and
benefits of mixed groups to birds and monkeys. Amer. 97. Primatol. 21:
87-100.
Terborgh, J. S., S. K. Robinson, T. A. Parker III, C.A. Munn and N. Pierpont.
1990. Structure and organization of an Amazonian forest bird commu-
nity. Ecol. Monogr. 60:213-238.
Thiollay, J. 1988. Comparative foraging success of insectivorous birds in
tropical and temperate forests: ecological implications. Oikos 53:17-30.

Thiollay, J. 1994. Structure, density and rarity in an Amazonian rainforest
bird community. J. Trop. Ecol. 10:449-481.
Thiollay, J. 1999. Frequency of mixed species flocking in tropical forest birds
and correlates of predation risk: an intertropical comparison. J.Avian Biol.
30: 282-294.
Thompson, J. N. and M. E Willson. 1979. Evolution of temperate bird/fruit
interactions: phenological strategies. Evolution 33: 973-982.
Titus, R. C., C. R. Chandler, E. D. Ketterson and V. Nolan Jr. 1997. Song
rates of dark-eyed juncos do not increase when females are fertile. Behav.
Ecol. Sociobiol. 41:165-169.
Trail, P. W. 1985. Courtship disruption modifies mate choice in a lek-
breeding bird. Science 227: 778-779.
Trail, P.W. 1990. Why should lek-breeders be monomorphic? Evolution 44:
1837-1852.
Trail, P.W. and E. S. Adams. 1989. Active mate choice at cock-of-the-rock
leks: tactics of sampling and comparison. Behav. EcoL Sociobiol. 25:
283-292.
Trivers, R. 1972. Parental investment and sexual selection. Pp. 136-179 In:
Sexual selection and the descent of man, 1871-1971 (B. Campbell, Ed).
Aldine, Chicago.
Tye, H. 1991. Reversal of breeding season by lowland birds at higher alti-
tudes in western Cameroon. Ibis 134:154-163.
Vanderwerf, E. 1992. Lack's clutch size hypothesis: an examination of the
evidence using meta-analysis. Ecology 73:1363-1374.
van Noordwijk, A. J., R. H. McCleery and C. M. Perrins. 1995. Selection for
the timing of great tit breeding in relation to caterpillar growth and tem-
perature. J. Anim. EcoL 64:451-458.
Verhencamp, S. L. 1978. The adaptive significance of communal nesting in
Groove-billed Anis (Crotophaga sulcirostris). Behav. Ecol. SociobioL 4: 1-33.
Verhulst, S., S. J. Dieleman and H. K. Parmentier. 1999. A tradeoffbetween
immunocompetence and sexual ornamentation in domestic fowl. Proc.
Natl.Acad. Sci. USA 96:4478-4481.
Verner, J. and M. F. Willson. 1966. The influence of habitats on mating
systems of North American passerine birds. Ecology 47:143-147.
Vleck, C. M. and J. L. Brown. 1999.Testosterone and social and reproductive
behaviour in Aphelocorna jays. Anirn. Behav. 58:943-951.
Wagner, R. H. 1993. The pursuit of extra-pair copulation by female birds: a
new hypothesis of colony formation. J. Theor. Biol. 163:333-346.
Wagner, R. H. 1998. Hidden leks: sexual selection and the clustering of avian
territories. Ornithol. Monogr. 49:123-145.
Wagner, R. H., M. D. Schug and E. S. Morton. 1996. Condition-dependent
control of paternity by female purple martins: implications for coloniality.
Weatherhead, P. J. and S. M.Yezerinac. 1998. Breeding synchrony and extra-
pair matings in birds. Behav. Ecol. Sociobiol. 40:151-158.
REFERENCES 157
Webster, M. S. 1995. Effects of female choice and copulations away from the
colony on fertilization success of male Montezuma Oropendolas (Psaro-
colius montezuma). Auk 112:659-671.
Webster, M. S. and S. K. Robinson. 1999. Courtship disruptions and male
mating strategies: examples from female-defense mating systems. Amer.
Nat. 154:717-729.
Werner, T. K. and T. W. Sherry. 1987. Behavioral feeding specialization in
Pinaroloxias inornata, the 'Darwin's Finch' of Cocos Island. Proc. Natl.
Acad. Sci. USA 84:5506-5510.
West-Eberhardt, M. J. 1983. Sexual selection, social competition and evolu-
tion. Q. Rev. Biol. 58: 155-183.
Westcott, D. 1997. Lek locations and patterns of female movement and dis-
tribution in a Neotropical frugivorous bird. Anim. Behav. 53: 235-247.
Wesmeat, D. F. and P.W. Sherman. 1993. Parentage and the evolution of
parental behavior. Behav. Ecol. 4: 66-77.
Wesmeat, D. F. and P.W. Sherman. 1997. Density and extra-pair fertiliza-
tions in birds: a comparative analysis. Behav. Ecol. Sociobiol. 41:205-215.
Westneat, D. F, P.W. Sherman and M. L. Morton. 1990. The ecology and
evolution of extra-pair copulations in birds. Curr. Ornithol. 7:331-369.
Wetmore, A. 1972. Birds of the Republic of Panama. Part 3. Smithsonian Inst.
Press, Washington.
Wetmore, A. 1984. Birds of the Republic of Panama. Part 4. Smithsonian Inst.
Press, Washington.
Wheelwright, N.T. 1986. The diet of American Robins: an analysis of the
U.S. Biological Survey records. Auk 103:710-725.
Wheelwright, N.T. 1988. Fruit-eating birds and bird-dispersed plants in the
tropics and temperate zone. Trends Ecol. Evol. 3: 270-274.
Whitney, B. M. and J. Alvarez Alonso. 1998. A new Herpsilochmus Antwren
(Aves: Thamnophilidae) from northern Amazonian Peru and adjacent
Ecuador: the role of edaphic heterogeneity of terra firme forest. Auk 115:
559-576.
Whittingham, L. A., P. D. Taylor and R. J. Robertson. 1992a. Confidence of
paternity and male parental care.Amer. Nat. 139:1115-1125.
Whittingham, L. A., A. Kirkconnell and L. M. Ratcliffe. 1992b. Differences
in song and sexual dimorphism between Cuban and North American
Red-winged Blackbirds (Agelaius phoeniceus). Auk 109: 928-933.
Wikelski, M., M. Hau and J. C.Wingfield. 1999a. Social instability increases
plasma testosterone in a year-round territorial neotropical bird. Proc.
Royal. Soc. Lond. B 266:551-556.
Wikelski, M., M. Hau, W. D. Robinson and J. C. Wingfield. 1999b. Seasonal
endocrinology of tropical passerines: A comparative approach. Pp
1224-1241 In: Proceedings of the 22nd Int. Ornithol. Congress (N. J. Adams
and R. H. Soltow, Eds) Birdlife South Africa, Johannesburg.
Wikelski, M., M. Hau, and J. C.Wingfield. 2000. Seasonality of reproduction
in a neotropical rainforest bird. Ecology, 81: 2458-2472.
Wiley, R. H. 1991. Associations of song properties with habitats for territor-
ial oscine birds of eastern North America. Amer. Nat. 138: 973-993.
Wiley, R. H. and M. S. Wiley. 1977. Recognition of neighbors' duets by
Stripe-backedWrens Campylorhynchus nuchalis. Behavior 62:10-34.
Wiley, R. H., R. Godard and A. D. Thompson. 1994. Use of two singing
modes by Hooded Warblers as adaptations for signalling. Behavior 129:
243-278.
Wilkinson, R. 1983. Biannual breeding and moult-breeding overlap of the
Chestnut-bellied Starling Spreo pulcher. Ibis 125:353-361.
Williams, M. and F. McKinney. 1996. Long term monogamy in a river spe-
cialist - the Blue Duck. Pp 73-90 In: Partnerships in birds: the ecology of
monogamy (J.M. Black, Ed.). Oxford Univ. Press, Oxford.
Willis, E. O. 1966. Competitive exclusion and birds at fruiting trees in
western Colombia. Auk 83: 479-480.
Willis, E. O. 1967.The behavior ofBicolored Antbirds. Univ. Calif. Publ. Zool.
79: 1-127.
Willis, E. O. 1972. The behavior of Spotted Antbirds. Ornithol. Monogr. 10:
1-162.
Willis, E. O. 1973. The behavior of Oscellated Antbirds. Smithsonian Contr.
Zool. 144:1-57.
Willis, E. O. 1974. Populations and local extinctions of birds on Barro
Colorado Island, Panama. Ecol. Monogr. 44: 153-169.
Willis, E. O. 1983. Longevities of some Panamanian forest birds, with note of
low survivorship in old Spotted Antbirds (Hylophylax naevioides). J. Field
Ornithol. 54:413-414.
Willis, E. O. 1985. Cercomacra and related antbirds (Aves, Formicariidae) as
army ant followers. Revta. Bras. Zool. 2: 427-432.
Willis, E. O. andY. Oniki. 1978. Birds and army ants. Ann. Rev. Ecol. Syst. 9:
243-263.
Willson, M. F. 1983. Avian frugivory and seed dispersal in eastern North
America. Curr. Ornithol. 3: 223-279.
Wilson, G. R. and M. C. Brittingham. 1998. How well do artificial nests
estimate success of real nests? Condor 100: 357-364.
Wingfield, J. C. 1984. Androgens and mating systems: testosterone-induced
polygyny in normally monogamous birds. Auk 101:665-671.
Wingfield, J. C. 1994. Regulation of territorial behavior in the sedentary song
sparrow, Melospiza melodia morphna. Horm. Behav. 28: 1-15.
Wingfield, J. C. andT. P. Hahn. 1994. Testosterone and territorial behaviour
in sedentary and migratory sparrows. Anim. Behav. 47: 77-89.
Wingfield, J. C. and D. M. Lewis. 1993. Hormonal and behavioral responses
to simulated territorial intrusion in the cooperatively breeding white-
browed sparrow weaver, Plocepasser mahali. Anim. Behav. 45:1-11.
Wingfield, J. C. and M. C. Moore. 1987. Hormonal, social, and environmen-
tal factors in the reproductive biology of free-living male birds. Pp
148-175 In: Psychobiology of reproductive behavior: an evolutionary perspec-
tive (D. Crews, Ed.). Prentice-Hall, Inc., New Jersey.
Wingfield, J. C., R. E. Hegner Jr, A. M. Dufty Jr. and G. F. Ball. 1990. The
REFERENCES 159
'challenge hypothesis': theoretical implications for patterns of testos-

terone secretion, mating systems, and breeding strategies. Amer. Nat. 136:
829-846.
Wingfield, J. C., R. E. Hegner and D. M. Lewis. 1992. Hormonal responses
to removal of a breeding male in the cooperatively breeding white-browed
sparrow weaver, Plocepasser mahali. Horm. Behav. 26:145-155.
Wingfield, J. C., J. D. Jacobs, K. Soma, D. L. Maney, K. Hunt, D. Wisti-
Peterson, S. Meddle, M. Ramenofsky and K. Sullivan. 1999.Testosterone,
aggression, and communication: ecological bases of endocrine phenom-
ena. Pp 255-283 In: The Design of Animal Communication (M. D. Hauser
and M. Konishi, Eds). MIT Press, Cambridge, Massachusetts.
Witmer, M. C. 1993. Cooperative breeding by Rufous Hornbills on
Mindanao Island, Philippines.Auk 110: 933-936.
Wittenberger, J. F. 1979. A model for delayed reproduction in iteroparous
animals. Amer. Nat. 114: 439-446.
Wittenberger, J. L. and R. L. Tilson. 1980. The evolution of monogamy:
hypotheses and evidence.Ann. Rev. Ecol. and Syst. 11: 197-232.
Wolf, L., E. D. Ketterson andV. Nolan Jr. 1988. Paternal influence on growth
and survival of dark-eyed junco young: Do parental males benefit? Anim.
Behav. 36:1601-1618.
Wolf, L. L. 1969. Female territoriality in a tropical hummingbird. Auk 86:
490-504.
Wolf, L. L. 1975. Female territoriality in the purple-throated carib. Auk 92:
511-522.
Woodall, E E 1994. Breeding season and clutch size of the noisy pitta Pitta
versicolor in tropical and subtropical Australia. Emu 94: 273-277.
Woodworth, B. L. 1997. Brood parasitism, nest predation, and season-long
reproductive success of a tropical island endemic. Condor 99:605-621.
Woodworth, B. L., J. Faaborg and W. J. Arendt. 1999. Survival and longevity
of the Puerto RicanVireo. Wilson Bull. 111: 376-380.
Wrege, E H. and S.T. Emlen. 1991. Breeding seasonality and reproductive
success of White-fronted Bee-eaters in Kenya. Auk 108: 673-687.
Wright, J. 1998. Paternity and paternal care. Pp 117-145 In: Sperm competi-
tion and sexual selection (T. R. Birkhead and A. P. Moiler, Eds). Academic
Press, London.
Wunderle, J. M. Jr. 1982.The timing of the breeding season in the bananaquit
(Coerebaflaveola) on the island of Grenada, W. I. Biotropica 14:124-131.
Wunderle, J. M. Jr. and K. H. Pollock. 1985.The banaquit-wasp nesting asso-
ciation and a random choice model. Ornithol. Monogr. 36: 595-603.
Wyndham, E. 1986. Length of birds' breeding season. Amer. Nat. 128:
155-164.
Yom-Tov, Y., M. I. Christie and G. J. Iglesia. 1994. Clutch size in passerines
of southern South America. Condor 96:170-177.
Young, B. E. 1994. The effects Of food, nest predation and weather on the
timing of breeding in tropical house wrens. Condor 96:341-353.
Young, B.E. 1996. An experimental analysis of small clutch size in tropical
house wrens. Ecology 77: 472-488.

Zack, S. 1990. Coupling delayed breeding with short-distance dispersal in
cooperatively breeding birds. Ethology 86: 265-286.
Zack, S. and J. D. Ligon. 1985a. Cooperative breeding in Lanius shrikes. I.
Habitat and demography of two sympatic species. Auk 102: 754-765.
Zack, S. and J. D. Ligon. 1985b. Cooperative breeding in Lanius shrikes. II.
Maintenance of group-living in a nonsaturated habitat. Auk 102:
766-773.
Zack, S. and K. N. Rabenold. 1989. Assessment, age and proximity in dis-
persal contests among cooperatively breeding wrens: field experiments.
Anim. Behav. 38: 235-247.
Zack, S, and B. J. Stutchbury. 1992. Delayed breeding in avian social
systems: the role of territory quality and 'floater' tactics. Behavior 123:
194-219.
Zahavi, A. 1975. Mate selection- a selection for handicap. J. Theor. Biol. 53:
205-214.
Zahavi, A. 1977. The cost of honesty (further remarks on the handicap prin-
ciple). J. Theor. Biol. 67: 603-605.
Zahavi, A. and A. Zahavi. 1997. The handicap principle. Oxford Univ. Press,
Oxford.
Zandt, H., A. Strijkstra, J. Blondel and J. H. Van Balen. 1990. Food in two
Mediterranean blue tit populations: do differences in caterpillar availabil-
ity explain differences in timing of the breeding season. Pp 145-155 In:
Population biology of passerine birds, an integrated approach (J. Blondel, A.
Gosler, J. D. Lebreton and R. McCleery, Ed.). Berlin: SpringerVerlag.
Index
Acrocephalus paludicola 98 Bananaquit 16

Acrocephalus sechellensis 15-16, 57 Bee-eater, White-fronted 10, 22
Aerodramusspodiopygius 32 Bellbird, Bearded 114
Aethia cristatella 104 benefits ofphilopatry 57-8
Agelaius phoeniceus 5, 69-70, 71, 99, Bentbill, Northern 54
104 birds of paradise 54-5
aggression, intersexual 104, 106 biodiversity: 3-4, 129-30
aggression, interspecific 105 Blackbird, Red-winged 5, 69-70, 71,
Akepa, Hawaii 26 99, 104
Anas bahamensis 49 Blackcap 84, 86
ant-followers 4, 66, 105 Bluebird, Eastern 88
Ant-Tanager, Black-cheeked 101 Bluethroat 83
Antbird, Bicolored 105 breeding synchrony 9, 20, 41-5,
Antbird, Dusky 8, 24, 26, 35, 41, 44, 51-2,
65, 71-8, 94-5, 100, 104, 115 breeding territoriality 61-3, 81
Antbird, Oscellated 105 brood manipulation 30-3, 35-6
Antbird, Sooty 63 Bunting, Indigo 91
Antbird, Spotted 21, 26, 40, 46, Buteogallus meridionalis 32
69-71, 73, 84
Antbird, White-bellied 74, 84 Cacicus cela 43, 94
Antshrike, Slaty 26, 33 Cacique, Yellow-rumped 43, 94
Antwren, Dot-winged 17 Campylorhynchus nuchalis 58
Antwren, Checker-throated 26, 68, Capuchinbird 104-5
73 Carib, Purple-throated 67
Antwren, Gray 127 Catbird, Gray 113
Antwren, Ihering's 127 Cercomacra tyrannina 8, 24, 26, 35,
Antwren, Long-winged 127 41, 44, 65, 71-8, 94-5, 100, 104,
Antwren, Plain-throated 127 115
Antwren, Pygmy 127 Cerylerudis 59
Antwren, White-eyed 127 Cettiacetti 98
Antwren, White-flanked 63, 127 Chamaea fasciata 96
Apane 13 Chickadee, Black-capped 45, 85
Aphelocomacalifornica 47 Chiroxiphia linearis 26
Aphelocomauhramarina 47 Cistothorus 96
Aquila wahlbergi 16 climatic constraints 11
Ashmole's hypothesis 32 clutch size 28-38,
Asite, Velvet 55 Cock-of-the-Rock, Guianan 104-5,
Auklet, Crested 104 122-4
Coereba flaveola 16
coevolution 109-10, 117 floater 27, 71-8

colouration 99-107, 121-4 Flycatcher, Collared 83
Columbia leucocephala 13 Flycatcher, Least 69
Columbiniapasserina 24 Flycatcher, Ochre-bellied 53
communication, assessement/manage- Flycatcher, Piratic 114, 118
ment 79-81, 88 Flycatcher, Vermillion 103
competition 33 food, nestling 115-16
competition, female-female 103-5 food availability 12-16, 19-20, 86-7
conservation 4, 45, 124, 129-30 food delivery rates 30, 33, 37
Corapipo gutturalis 122-4 food limitation hypothesis 28-33
cost of reproduction 34-6, 38 food supplementation 86,
Creagrusfurcatus 32 foraging styles 124-9
Cyanocompsa cyanoides 94-5 Forpus passerinus 26-7, 28, 32, 35, 41
C3~horinusphaeocephalus 22,47 frugivorous 2, 12-13, 53, 58, 62, 66,
110-17
dawn chorus 20, 83-5, 87 fruit abundance 110-11
dead leaf foraging 125, 127 fruit-influenced territories 62-3, 66
delayed breeding 56-60, 101
Dendroica adelaidae 84 Geospiza 13, 26, 41
Dendroica castanea 120 Glaucis hirsuta 24
Dendroica pensylvanica 120 good genes 43, 84
Dendroica tigrina 118 granivorous 12, 53, 114
density 45 Grassquit, Blue-black 42
differential allocation hypothesis 50 Greenlet, Lesser 120
dispersal 56-8 Grosbeak, Blue-black 94-5
Dove, Plain Ground 24 Grosbeak, Rose-breasted 113
dry season 1-3, 11, 19 growls 80
ducks 49-50 growth rates 28
duetting 88, 89-90 Gull, Swallow-tailed 32
Dumetella carolinensis 113 Gymnopithys leucaspis 105
Eagle, Wahlberg's 16 Habia atrimaxillaris 101

egg laying 34 habitat saturation 57-8, 59-60
Elaenia, Lesser (Elaenia chiriquensis) Hawk, Savannah 32
51-2, 64, 114, 116 helping 58-9
Elaenia,Yellow-bellied (Elaenia flavo- Henicorhina leucosticta 89-92
gaster) 51-2, 84, 116 Hermit, Long-tailed 13-14, 17, 26,
Empidonax minimus 69 Hermit, Rufous-breasted 24
Erithacus rubecula 89 Himatione sanguinea 13
Eulampis jugularis 67 Hirundo rustica 5
Euphonia, Yellow-throated (Euphonia hummingbirds 66-7, 102, 106
hirundinacea) 28 Hylophilusminor 120
extra-pair mating 6-7, 39-52, 59, Hylophylax naevioides 21, 26, 40, 46,
67-71, 81-7, 101 69-71, 73, 84
Ficedulaalbicollis 83 Icterus spurius 118

Finch, Cocos 127 Iiwi 13
Finches, Darwin's 13, 26, 41 immunocompetence 106-7
INDEX 163
information transfer 79-81 120, 124-9

insect abundance 30, 110-11 Mockingbird, Northern 116
insectivorous 2, 12-13, 53, 62-6, molt 17, 119-20
intrusion rate 52 monogamy 39-52
Myrmecizafortis 63
Jacana, Wattled (Jacanajacana) 48 Myrmeciza longipes 74, 84
Jay, Mexican 47 Myrmotherula axillaris 63, 127
Jay, Western Scrub 47 Myrmotherula brachyura 127
Myrmotherulafulviventris 26, 68, 73
kin selection 58-9 Myrmotherula hauxwelli 127
Kingbird, Eastern 119 Myrmotherula iheringi 127
Kingfisher, Pied 59 Myrmotherula leucophthalma 127
Kite, Snail 32 Myrmotherula longipennis 127
Myrmotherula menetriesii 127
Lanio versicolor 129
Lanius 57, 60 necatarivorous 12-13, 66-7
Legatus leucophaius 114, 118 neighborhood stability 65, 86, 89,
lek 40, 42, 52-5, 102, 104, 121-4 93-9
Lepidothrix serena 102, 122-4 nest building 52
life history tradeoffs 34-6 nest defense 52
light environment 121-4 nonbreeder 27, 71-8
Loxiodes bailleui 41 nuclear species 102, 127
Loxops coccineus 26
Luscinia svecica 83 Oncostoma cinereigulare 54
Oporornis formosus 88
Manakin, Long-tailed 26 Oriole, Orchard 118
Manakin, Golden-collared (Manacus Oropendola, Montezuma 43
vitellinus) 47
Manakin, White-bearded (Manacus pair formation 45, 77
manacus) 25-6, pairing success 52
Manakin, White-collared (Manacus Palila 41
candez) 13-14 parasites 107
Manakin, White-fronted 102, 122-4 parental care 33, 41, 48-51, 53-5,
Manakin, White-throated 122-4 106
Martin, Purple 94 Parrotlet, Green-rumped 26-7, 28,
mate choice 50-1, 77, 82, 106-7 32, 35, 41
mate guarding 40, 52 Parus caeruleus 5, 11, 12
Melanerpes formicivorus 58 Parus major 11
Melospiza melodia 69, 96 Passerina cyanea 91
Merops bullockoides 1O, 22 Perissocephalus tricolor 104-5
Microrhopias quixensis 17 Phaenostictus mcleannani 105
migrants 88-9, 95-6, 106, 117-21, Phaethornis superciliosis 13-14, 17, 26,
126 Pheucticus ludovicianus 113
migrants, altitudinal 1 Philepittacastanea 55
migrants, intra-tropical 1, 114, 118 photoperiod 21
Mimus polyglottus 116 Picoides pubescens 126
Mionectes oleagineus 53 Pigeon, White-crowned 13
mixed species flocks 63, 65-6, 73, Pinaroloxiasinornata 127
Pintail, White-cheeked 49 southern hemisphere 36-8, 49-50

Piranga olivacea 113, 119 species diversity 3-4
Piranga rubra 119 sperm competition 39-40, 47
Pitohui 121 survival, adult 25-8, 34-6
Plocepassermahali 70 Swallow, Barn 5
plumage, subadult 100-1 Swallow, Mangrove 10, 40-1
plumage coloration 99-107, 121-4 Swallow, Tree 40
plumage manipulation 99 Swiftlet, White-rumped 32
Poecile atrica_pillus 45, 85 Sylvia atricapilla 84, 86
predation, adult 74, 106-7, 121-9
predation, nest 16-17, 23-5, 33-4, Tachycineta albilinea 10, 40-1
37, 106-7, 115 Tachycineta bicolor 40
Procnias averano 114 Tachyphonus luctuosus 63, 101
Progne subis 94 Tanager, Bay-headed 101
promiscuity 52-5 Tanager, Black-faced 101
Psarocolius montezuma 43 Tanager, Blue-gray 47
Pyrocephalus rubinus 103 Tanager, Scarlet 113, 119
Tanager, Summer 119
removal experiments 8, 55, 71-8, Tanager, White-shouldered 63, 101
reproductive effort 34-6 Tangara gyrola 101
resource holding potential 71-2 temperate zone bias 4-6
Robin, American 116 terrioriality, interspecific 65, 67, 102
Robin, Clay-colored 11, 16, 18-21, territory acquisition 8, 34, 71-8
30-2, 40, 41, 46, 64, 83-4, 115 territory defense 7-8, 67-72, 81-9,
Robin, European 89 126-7
Rostrhamussociabilis 32 territory establishment 69
Rupicola rupicola 104-5, 122-4 territory intrusions 68
territory quality 65, 76-7
Schistochlamys melanopis 101 territory size 63-4, 126
seasonality 9 territory stability 64-5
sex roles 48-51, 87-9, 103-7 territory switching 64, 75-8
sexual dimorphism 67, 101-7 territory types 62-7
sexual selection 18-21, 50 testes size 39-40, 51-2
Skutch's hypothesis 33-4, 37 testosterone 7, 46-8, 69-71, 107-8
Shrike-Tanager, White-winged 129 Thamnophilus atrinucha 26, 33
Shrikes 57, 60 Thraupisepiscopus 47
Sialia sialis 88 Thryothrorus eisenmanni 103
Sparrow, Rufous-collared 10, 60, 72 Thryothorus leucotis 50, 74-8, 83
Sparrow, Song 69, 96 Thryothorus ludovicianus 86, 87, 92,
Sparrow, White-crowned 70, 96, 97 96-8
song, dialect 91-9 Thryothorusnigricapillus 75
song, female 87-9 Tit, Blue 11, 12
song, function 81-7, 93 Tit, Great 5, 11
song, repeat mode 98 Troglodytes aedon 14-15, 17, 32, 33,
song matching 96 35,73,77
song output 68, 70, 77, 82-7 Turdus grayi 11, 16, 18-21, 30-2, 40,
song ranging 89-99 41, 46, 64, 83-4, 115
song repertoire 91-9 Turdus migratorius 116
INDEX 165
Tyrant-Manakin, Dwarf (Tyranneutes Warbler, Kentucky 88

stolzmannz) 63 Warbler, Seychelles 15-16, 57
Tyrannus tyrannus 119 Warbler, Tennessee 118, 120
Weaver, White-browed Sparrow 70
ultraviolet 102 wet season 1-3, 11
White-eye 41
Vermivora peregrina 118, 120 Wilsonia citrina 1O, 35, 44, 67, 83
Vestaria coccinea 13 Wood-wren, White-breasted 89-92
Vireo, Blue-headed (Vireo solitarius) Woodpecker, Acorn 58
50 Woodpecker, Downy 126
Vireo, Mangrove (Vireopallens) 120 Wren, Bay 75
Vireo, White-eyed (Vireo griseus) 89, Wren, Buff-breasted 50, 74-8, 83
119, 120 Wren, Carolina 86, 87, 92, 96-8
Vireo, Yellow-green ( Vireoflavoviridis) Wren, Inca 103
114, 118 Wren, Song 22, 47
Volatinia jacarina 42 Wren, Stripe-backed 58
Wren, Tropical House 14-15, 17, 32,
Warbler, Adelaide's 84 33,35,73,77
Warbler, Aquatic 98 wren, Sedge 96
Warbler, Bay-breasted 120 Wrentit 96
Warbler, Bush 98
Warbler, Cape May 118 Zonotrichia capensis 10, 60, 72
Warbler, Chesmut-sided 120 Zonotrichia leucophrys 70, 96, 97
Warbler, Hooded 10, 35, 44, 67, 83 Zosteropslateralis 41

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Preface

1.1 Ecology and breeding seasons

1.3 Temperate zone bias in behavioral ecology

tropical species (e.g. Greenberg and Gradwohl 1983). These typical

1.4 Examples of temperate zone bias

relatively u n c o m m o n in socially monogamous tropical birds and,

Testosterone and territory defense

Interest in what controls the timing of breeding in birds goes back to

2.1 Seasonality in tropical breeding seasons

2.2 Food availability and timing of breeding

comparisons, which lump many species together into ecological

breeding vacancies scarce (see Chapter 5), reproductive success may be

2.3 Nest predation and molt

Nest predation does not explain all examples of early breeding by

2.4 Sexual selection and the breeding season of the

Pacific coast, near Panama City, than 20 km inland at Summit

flight feathers by young robins must be an adaptation to their starva-

nothing about the fimess consequences of different individual strate-

It has long been recognized that tropical birds differ fundamentally

3.1 High nest predation

Nest predation in the tropics likely varies with habitat (Marchant

3.2 High adult survival

Species Years N Survival (%)

White-bearded Manakin a 9 182 82%

Parrotlet, Forpus passerinus (Sandercock et al. 2000), where survival

Johnston et al. (1997) estimated the annual survival of tropical forest

A powerful test is to compare survival in a genus that occurs in both

3.3 Small clutch size

being insectivorous, the Trumpet Manucode is strictly frugivorous

4.5 Cooperative breeding

Why stay at home?

breeding vacancies that can be filled by young birds (Brown 1987).

Zack and Rabenold (1989) found that in Stripe-backedWrens, Campy-

Why isn't cooperative breeding more common in the tropics?

not breeding at all. Many of the cooperative breeders studied to date

Latitudinal differences in territorial behavior in relation to breeding

temperate zone model, which is constrained by climate and so driven

5.1 Territory systems

Type o f Territory a Number o f species Number o f genera b

1. many types of lek and cooperative breeding examples,

In mixed flocks of the forest interior insectivorous type, many species

usually cooperate in defending the territory (Greenberg and Gradwohl

sometimes defend seemingly excessive territories, and have very low

hummingbirds. This interspecific territoriality means that males can

5.2 Territory defense

tropical passerines are due to influences of extra-pair behavior. In tem-

patterns. Females prefer to settle on territories where extra-pair males

Testosterone and territoriality

Zonotrichia leucophrys (Hau et al. 2000). Testosterone in Spotted

levels of testosterone, seen routinely in temperate zone birds, carry a

Resource holding potential

and ousting their replacements, if any. Removed residents, in contrast,

5.3 Territory acquisition

In tropical House Wrens, Troglodytes aedon, floaters of both sexes are

5.4 Territory switching

Wren, about 15% of adults switch territories during their lifetime,

switching in Dusky Antbirds and Buff-breasted Wrens to very little

6.1 The assessment/management concept in