(Current Ornithology 6) Randall Breitwisch (Auth.), Dennis M. Power (Eds.) - Current Ornithology-Springer US (1989) PDF

CURRENT
ORNITHOLOGY
VOLUME 6
Current Ornithology
Editorial Board
George F. Barrowclough, American Museum of Natural History,

New York, New York
Robert E. Ricklefs, University of Pennsylvania, Philadelphia, Pennsylvania
Stephen I. Rothstein, University of California, Santa Barbara, California
Ralph W. Schreiber, Los Angeles County Museum of Natural History,
Los Angeles, California
John A. Wiens, Colorado State University, Fort Collins, Colorado
A Continuation Order Plan is available for this series. A continuation order will bring
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CURRENT
ORNITHOLOGY
VOLUME 6
Edited by
DENNIS M. POWER
Santa Barbara Museum of Natural History
Santa Barbara, California
Springer Science+ Business Media, LLC

The L i b r a r y of Congress cataloged the first volume of this title as follows:
Current o r n i t h o l o g y . - V o l . 1 -
N e w York: Plenum Press, C1983-
v.: i l l . ; 24 c m .
Annual.
Editor: R i c h a r d F. Johnston.
ISSN 0742-390X = C u r r e n t ornithology.
1. Ornithology—Periodicals. I. Johnston, Richard F.
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ISBN 978-1-4757-9920-0 ISBN 978-1-4757-9918-7 (eBook)

DOI 10.1007/978-1-4757-9918-7
© 1989 Springer Science+Business Media New York

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CONTRIBUTORS
RANDALL BREITWISCH, Department of Biology, University of Miami,

Coral Gables, Florida 33124. Present address: Department of
Biology, University of Dayton, Dayton, Ohio 45469
GREGORY S. BUTCHER, Department of Zoology and Burke Museum,

University of Washington, Seattle, Washington 98195. Present
address: Cornell Laboratory of Ornithology, Ithaca, New York 14850
PAUL KERLINGER, Cape May Bird Observatory, Cape May Point, New
Jersey 08212
GABOR 1. LOVEI, Laboratory of Functional Ecology, Department of

Zoology, Plant Protection Institute, Hungarian Academy of Sci-
ences, Budapest, H-1525 Hungary
FRANK R. MOORE, Department of Biological Sciences, University of

Southern Mississippi, Hattiesburg, Mississippi 39406-5018
SIEVERT ROHWER, Department of Zoology and Burke Museum, Uni-

versity of Washington, Seattle, Washington 98195
NOEL F. R. SNYDER, Portal, Arizona 85632
HELEN A. SNYDER, Portal, Arizona 85632
JERRY A. WALDVOGEL, Section of Neurobiology and Behavior, Cor-

nell University, Ithaca, New York 14853
v
PREFACE
This edited series has three principal goals. The first is to provide
information in a relatively concise way for researchers needing an over-
view of specific disciplines. The second is to provide an update on
specific schools of thought, bringing together ideas from colleagues
whose works often appear in a variety of journals. And the third is to
stimulate and suggest directions for new research. Volume 6 continues
the tradition established by the previous editor and editorial board in
providing new information, updating our understanding of specific dis-
ciplines, and stimulating new research.
In the first chapter, Randall Breitwisch examines mortality patterns
and sex ratios in monogamous birds. He argues that there are many
more components to measuring parental investment than are often re-
alized; our knowledge is weak in several areas. Understanding the evo-
lution of mating systems depends on better distinguishing the different
intensities of natural selection that operate on males and females. Greg-
ory Butcher and Sievert Rohwer develop a framework for assessing the
role of colorfulness in birds. They propose several hypotheses to test
and advocate evaluating more than one hypothesis at a time. Future
work on the evolution of distinctive coloration and of sexual and age
dimorphism must take these ideas into account.
Paul Kerlinger and Frank Moore examine the structure of the at-
mosphere (e.g., thermals, winds, temperature) as it may be relevant to
avian migration. They develop the hypothesis that atmospheric struc-
ture is an important force in natural selection for timing and altitude
of migration. A comparison is made with other presumed selective
vii
viii PREFACE
influences, such as predation and competition. Gabor Lovei of Hungary

shares his review of passerine migration between the Palaearctic and
Africa, allowing comparisons to be made with the Nearctic-Neotropical
system. Geographic barriers for birds migrating from Europe and Asia
to Africa are greater than those existing between North and South Amer-
ica; these barriers influence the patterns of passerine migration.
Noel and Helen Snyder summarize their knowledge of the biology
of the California Condor and the history and issues that led to conser-
vation efforts and capture of the last remaining birds. They reveal the
fascinating undercurrent of politics and interactions driving the de-
velopment of decisions affecting endangered species. The prospects
ahead for captive breeding and release of condors in the wild, and the
ultimate goals for condor conservation, are addressed. Jerry Waldvogel
concludes the volume with an excellent synopsis of olfaction in birds
and the growing body of research that suggests smell may be used in
orientation and navigation. Much of the work in Italy, Germany, and
the United States focuses on navigation in homing pigeons. The debate
over different results obtained for seemingly similar experiments is
intriguing and indicates that this field of study is extremely active at
present.
Volume 6 marks a change in the editorship of Current Ornithology.
The new editor and editorial board intend to build on the solid founda-
tion created by the;previous editor, Richard F. Johnston, and his capable
editorial board. We thank him for handing over the series in such fine
condition. Our goal is to provide substantial papers on what is timely
in avian research. We also want to foster an exchange of ideas among
ornithologists from around the world and plan to include the writings
of researchers in countries from outside what we, in the narrower per-
spective of most of our reading, perceive to be the mainstream. Mono-
graphs and studies of a length greater than what most journals may find
comfortable also will be featured. We invite your comments and crit-
icisms.
As this preface was being written the editor learned of the untimely
passing of one of the members of his editorial board, Ralph W. Schrei-
ber. To his memory, in respect of his substantial contribution to the
field of ornithology, the volume is dedicated.
Dennis M. Power
Santa Barbara, California
CONTENTS
CHAPTE}{ 1
MORTALITY PATTERNS, SEX RATIOS, AND PARENTAL INVESTMENT IN

MONOGAMOUS BIRDS
RANDALL BREITWISCH
1. Introduction ......................................................... 1
2. Sex Ratios ........................................................... 3
2.1. Sex Ratios in Eggs............................................. 4
2.2. Sex Ratios in Nestlings and Fledglings ..................... 4
2.3. Sex Ratios in Juveniles ....................................... 6
2.4. Sex Ratios in Adults .......................................... 7
3. Mortality Patterns................................................... 10
3.1. Juvenile Mortality............................................. 11
3.2. Age-Independent Mortality................................... 14
3.3. Conclusions ..................... < •••••••••• " •• •••••• •• •• •••• •• 17
4. Male and Female Parental Investment.. . . . . . . . . . . . . .. . . . . . . . . . . . . 18
4.1. The Problem of Currency..................................... 20
4.2. Female Parental Investment.................................. 21
4.3. Male Parental Investment .................................... 25
4.4. Further Complications ........................................ 28
4.5. Case Histories.................................................. 28
4.6. Conclusions .................................................... 33
5. Discussion ........................................................... 34
5.1. Testing Predictions of Alternative Hypotheses.. ... . .. .. ... 34
ix
x CONTENTS
5.2. Why Aren't More Birds Polyandrous? ...................... 37

5.3. Conclusions and Prospectus ................................. 39
References ........................................................... 40
CHAPTER 2
THE EVOLUTION OF CONSPICUOUS AND DISTINCTIVE COLORATION FOR

COMMUNICATION IN BIRDS
GREGORY S. BUTCHER AND SIEVERT ROHWER
1. Introduction ......................................................... 51
1.1. Classifying Coloration: Conspicuous, Distinctive,
or Cryptic ...................................................... 53
1.2. A Brief History of Color Hypotheses ........................ 56
2. The Three Rules of Avian Color Dimorphism ................... 57
3. The Three Rules and the Threat Hypothesis ..................... 59
4. Variability, Monomorphism, and the Threat Hypothesis....... 62
4.1. Monomorphism ............................................... 62
4.2. Between-Class Variability .................................... 63
4.3. Within-Class Variability ...................................... 64
5. Color Dimorphisms/Polymorphisms Independent of Sex,
Age, and Season .................................................... 65
6. Contrasting the Hypotheses ........................................ 69
6.1. Physiology or Communication............................... 69
6.2. Signaling to Conspecifics, Predators, or Prey. . . . . . .. .. . . .. . 70
6.3. Breeding or Nonbreeding Adaptation....................... 75
6.4. Agonistic or Epigamic Species Recognition ................ 79
6.5. Agonistic or Epigamic Sexual Selection .................... 83
6.6. Mate Choice or Mate Attraction ............................. 87
6.7. Agonistic Presence or Quality ............................... 92
7. Conclusions ......................................................... 95
References ........................................................... 97
CHAPTER 3
ATMOSPHERIC STRUCTURE AND AVIAN MIGRATION
PAUL KERLINGER AND FRANK R. MOORE
1. Introduction ......................................................... 109

2. Atmospheric Structure ............................................. 110
2.1. Vertical Wind .................................................. 111
2.2. Horizontal Wind ............................................... 114
2.3. Temperature and Relative Humidity Fluctuations ......... 116
CONTENTS xi
3. Predictions .......................................................... 117

3.1. Diel Timing .................................................... 117
3.2. Altitude ........................................................ 120
4. Flight Behavior: Test' of Predictions .............................. 121
4.1. Diel Timing of Migration ..................................... 121
4.2. Altitude of Migration ......................................... 124
5. Fit of the Data to Predictions ...................................... 126
6. The Daytime Feeding and Predator-Avoidance Hypotheses .... 129
7. Summary ............................................................ 130
References ........................................................... 136
CHAPTER 4
P ASSERINE MIGRATION BETWEEN THE P ALAEARCTIC AND AFRICA
GABOR L. LOVEI
1. Introduction ......................................................... 143

2. Long-Term Fluctuations in the Palaearctic and Africa .......... 144
3. The African Continent: Fauna and Resources ................... 146
3.1. Faunal Relationships .......................................... 146
3.2. Vegetation Belts in Africa: Their Importance to Migrants 148
3.3. Rainfall and Resource Fluctuation Patterns ................ 150
4. Behavior of the Migrants ........................................... 151
4.1. Regulation of Migratory Behavior ........................... 151
4.2. Preparation for Migration: Fattening ........................ 152
4.3. Migratory Routes .............................................. 154
4.4. Overcoming Geographical Barriers .......................... 156
4.5. Recurrence ..................................................... 158
5. Migrants on Their Wintering Grounds ........................... 159
5.1. Wintering in the Mediterranean ............................. 159
5.2. Resource Use by Migrants in Africa ......................... 162
5.3. Migrants and the Local Avifauna ............................ 165
6. Conclusions ......................................................... 167
7. Summary ............................................................ 168
References ........................................................... 169
CHAPTER 5
BIOLOGY AND CONSERVATION OF THE CALIFORNIA CONDOR
NOEL F. R. SNYDER AND HELEN A. SNYDER
1. Introduction ......................................................... 175

2. History of Biological Studies ...................................... 177
xii CONTENTS
2.1. The Pre-Koford Era ............................................ 178

2.2. The Koford Era ................................................ 181
2.3. The McMillan years .......................................... 185
2.4. The Sibley Years .............................................. 188
2.5. The Wilbur Era ................................................ 190
2.6. The Modern Research Program .............................. 195
3. History of Condor Conservation ................................... 216
3.1. The Condor as a Symbol of Wilderness: The
Controversies of the 1940s and 1950s ....................... 217
3.2. Conservation and Controversies of the 1960s .............. 226
3.3. The 1970s: Transition to an Intensive Approach .......... 233
3.4. The Modern Conservation Program ......................... 234
4. The Road Ahead .................................................... 244
4.1. Prospects for Success in Captive Breeding ................. 244
4.2. Prospects for Release of California Condors to the Wild 246
4.3. Ultimate Goals of Condor Conservation .................... 251
5. Discussion ........................................................... 254
References ........................................................... 263
CHAPTER 6
OLFACTORY ORIENTATION BY BIRDS
JERRY A. WALDVOGEL
1. Introduction ......................................................... 269

2. Types of Orientation ............................................... 271
3. Avian Olfactory Sensitivity ........................................ 272
3.1. Early Attempts to Study Avian Olfaction ................... 273
3.2. Olfactory Thresholds .......................................... 274
4. Chemical and Atmospheric Influences on Olfactory
Orientation .......................................................... 277
4.1. Natural Sources of Odors ..................................... 277
4.2. Mechanisms of Odor Dispersion ......... , ................... 280
5. Behavioral Evidence for the Use of Odors in Avian
Orientation .......................................................... 287
5.1. Odors as Landmarks .......................................... 287
5.2. Can Odors Provide a Reliable Compass? .................... 297
5.3. True Olfactory Navigation .................................... 301
6. Conclusions .................. , ...................................... 312
References ........................................................... 314
INDEX .................................................................... 323

CHAPTER 1
MORTALITY PATTERNS, SEX

RATIOS, AND PARENTAL
INVESTMENT IN MONOGAMOUS
BIRDS
RANDALL BREITWISCH
The females of some birds appear to die

earlier than the males
Darwin, 1871
1. INTRODUCTION
A subject of great interest to students of animal mating systems over

the past 15 years has been parental investment, a concept that includes
parental care and the cost of gametes, Parental care in birds (and other
animals) had been studied for many years prior to Trivers's (1972)
seminal paper, but Trivers's contribution was of major importance be-
cause he placed parental care in a theoretical framework. Specifically,
he attempted to link parental care to mortality patterns and sex ratios,
and thereby account for the varying strength of sexual selection in a
RANDALL BREITWISCH • Department of Biology, University of Miami, Coral Gables,

Florida 33124. Present address: Department of Biology, University of Dayton, Dayton,
Ohio 45469.
2 RANDALL BREITWISCH
diversity of mating systems. Parental investment (PI) is defined as "any

investment by the parent in an individual offspring that increases the
offspring's chance of surviving (and hence reproductive success) at the
cost of the parent's ability to invest in other offspring" (Trivers, 1972).
This definition has been modified to apply to clutches or broods of
offspring (Wi ttenberger, 1981).
Trivers (1972) characterized monogamous birds as displaying greater
levels of PI by females than by males and hypothesized that this dif-
ference followed evolutionarily from the initial disparity in gamete size
(however, see Beissinger, 1987). He suggested that male-biased adult
sex ratios apparently common in monogamous birds are attributed to
relatively high female reproductive effort, hence high female PI, yield-
ing lower survivorship in adult females than in adult males. He viewed
this differential mortality as occurring entirely in the nonbreeding sea-
son or, alternatively, anytime after the current breeding season. Birds
have been a popular group for the student of PI. This is because, al-
though monogamy and biparental care are exceedingly common in birds
(Kendeigh, 1952; Lack, 1968a; Skutch, 1976; Gring, 1982), there is con-
siderable interspecific variation in the relative contributions of males
and females to parental care (Wittenberger and Tilson, 1980; Gring,
1982; Mock, 1985; Silver et aI., 1985).
This chapter reviews information on mortality patterns for the sexes
in monogamouS', biparental birds, seeking temporal patterns in the aris-
ing of male-biased sex ratios. It is concluded that there is substantial
evidence that these skewed sex ratios arise either in juveniles, prior to
first breeding, or in adults in nonbreeding seasons, or both. As a result,
a reinterpretation of avian PI patterns is offered, stressing the scarcity
of females due to causes not related to PI. The general scarcity of females
in populations may then allow surviving females to demand high levels
of paternal care of offspring (Breitwisch et aI., 1986b; Breitwisch, 1988).
Finally, there is some evidence that males in biparental, mono-
gamous birds contribute substantial care in populations in which adult
females are scarce.
There are three hypotheses regarding the origin of male-biased
adult sex ratios in monogamous birds. Females may become relatively
limited via differential mortality as (1) juveniles, (2) adults from non-
reproductive causes, or (3) adults from PI. The first and second hy-
potheses are not mutually exclusive. If either is true, the prediction is
that males will display high levels of PI. If the third hypothesis is true,
then, by definition, females are expending high PI.
Three kinds of data pertinent to testing among these three hy-
potheses are discussed. The relevant data are (1) the evidence for equal-
ity in sex ratios of offspring until the end of parental care, yet male-
SEX RATIOS AND PARENTAL INVESTMENT
biased sex ratios of breeding adults, (2) mortality patterns of the sexes,
and (3) patterns of male and female parental investment.
2. SEX RATIOS
Unbalanced sex ratios in populations of adult birds were once

believed responsible for determination of mating systems; e.g., an ex-
cess of males would lead necessarily to polygyny (e.g., Skutch, 1935,
1976; Mayr, 1939; Armstrong, 1965). Recently, the potential relevance
of skewed population sex ratios seems to have been relegated to minor
importance, subsequent to recognition of the major importance of re-
source availability, richness, and defensibility to the favoring of par-
ticular mating systems (however, see Rowley, 1981; Lamprecht, 1987;
and especially Murray, 1984). In place of the population sex ratio, the
"operational sex ratio" has been emphasized, i.e., "the average ratio of
fertilizable females to sexually active males at any given time" (Emlen,
1976; Emlen and Oring, 1977). Furthermore, interest in unbalanced sex
ratios was dampened by acceptance of Fisher's (1958) argument for the
evolutionary stability of equal investment in the sexes, usually resulting
in sex ratios of unity, except, perhaps, for sexually size dimorphic
species. Finally, the suggestion that sex ratios in monogamous birds
become male-biased in adults as a result of relatively high PI by females
appears to have been largely accepted. In sum, these arguments have
led to the view that adult sex ratios are simply the result of other, more
important, factors and do not causally determine mating systems or
parenting patterns.
This section reviews the available information on male-biased sex
ratios in birds, concentrating on monogamous passerines. Causes of
mortality are subsequently discussed, although sex ratios must ob-
viously be the result of male and female mortality schedules. This
arbitrary division is employed for two reasons: (1) to emphasize the
similar temporal pattern among species in the arising of male-biased
sex ratios, and (2) to examine separately the sources of mortality, seek-
ing common causes of differential mortality between the sexes. Infor-
mation from several life-history stages is examined: (1) eggs, (2) nest-
lings, (3) at the termination of parental care, (4) juveniles prior to the
first breeding, and (5) adults. It is concluded that, although there is
substantial evidence for skewing of sex ratios in adult birds, we lack
support for the assumption that this is a result of high female PI. Second,
there is some support for alternative, not mutually exclusive, hy-
potheses that sex ratios become male biased either before the age of
first breeding but after the termination of parental care, or in adults
from non-PI causes.
2.1. Sex Ratios in Eggs

Sex ratios at the egg-hatching stage do not differ from unity in
nearly all species of birds studied (Bellrose et 01.,1961; Williams, 1979;
Charnov, 1982; Clutton-Brock, 1986; Slagsvold et 01., 1986), although
the number of species examined is still rather small. Presumably, this
implies unity in primary sex ratios, i.e., equal numbers of fertilized
ova. Fiala (1981b) noted that birds have relatively few means of varying
primary sex ratios. Indeed, Williams (1979) suggested that there is no
strong evidence that birds (or mammals) are able to shift sex ratios in
clutches away from the random, Mendelian determination of sex, [al-
though Charnov (1982) disagrees; see also Burley (1982), Harmsen and
Cooke (1983), Mead et 01., (1987)]. The strongest evidence for primary
sex ratio adjustment in birds comes from work on Common Grackles
(Quiscalus quiscula) (Howe, 1977a) and Red-winged Blackbirds (Age-
laius phoeniceus) (Fiala, 1981a,b; see also Gowaty and Lennartz, 1985).
Howe (1977a) found a seasonal pattern of change in primary sex ratios,
with the proportion of females within clutches declining during the
breeding season. He suggested the mechanism to be nonrandom seg-
regation of the sex chromosomes. Clutton-Brock (1986) briefly dis-
cussed studies that have demonstrated variation in sex ratios in clutches
at or immediately after hatching. Reproductive and/or environmental
variables possibly related to this variation include order in clutch, order
of clutch in season, clutch size, egg weight, female age, habitat quality,
date of laying or hatching, season of hatching, and paternal breeding
success. Overall, however, there is little evidence for adaptive shifts in
sex ratios at hatching in birds.
2.2. Sex Ratios in Nestlings and Fledglings

Fisher's (1958) theory of the evolution of sex ratios predicts equal
investment in the sexes, culminating at the termination of parental care
(the secondary sex ratio). There is a serious logistical problem in testing
this prediction insofar as young passerines are cared for by their parents
after the young fledge, yet observations of parental care during the
fledgling period can be very difficult. Passerine fledglings tend to hide
in undergrowth during much of this final period of dependence; thus,
changes in sex ratios of offspring may not be recorded. Perhaps for this
reason, investigators have ascertained sex ratios in older nestlings just
prior to fledging and have claimed that this provides a test of Fisher's
prediction. It should be noted, however, that nestling sex ratios might
differ from sex ratios at the termination of parental care (see R0skaft
SEX RATIOS AND PARENTAL INVESTMENT 5
and Slagsvold, 1985, and Slagsvold et 01., 1986, for rooks Corvus frug-
ilegus). This possibility warrants investigation because many species
provide substantial parental care of fledglings. Thus, the opportunity
exists for differential care and/or mortality of the sexes during this final
period of dependence. In Song Sparrows (Melospiza melodia) and
Northern Mockingbirds (Mimus polyglottos), for instance, offspring re-
ceive more food from parents as fledglings than they do as nestlings 0.
Smith, 1978; Zaias and Breitwisch, 1988). Many other species display
relatively long fledgling periods (e.g., Newton, 1973), and significant
parental care of fledglings probably is the rule in monogamous passer-
ines.
Nearly all available evidence indicates that sex ratios at the nestling
stage are unity in birds. The exceptions appear to be species displaying
sexual size dimorphism, in which there may be departure from unity
with a predominance of the smaller (less expensive) sex. In most pas-
serines that display such dimorphism, males are larger than females;
thus, equal investment in the sexes (Fisher, 1958) results in a predom-
inance of females (Howe, 1977a; Fiala 1981a,b, and references cited
therein). Skewed sex ratios in these cases probably arise during the
nestling stage rather than in the primary sex ratio (Williams, 1979).
Conditions of food shortage may affect male and female nestlings
differentially in dimorphic species. In Great Tits (Parus major), for
example, (smaller) female nestlings suffer higher mortality than the
larger males, shifting secondary sex ratios (Dhondt, 1970; Perrins, 1979).
In several other species, food shortage appears to lead to greater mor-
tality of (larger) male nestlings (Clutton-Brock, 1986, and references
cited therein).
Clearly, sexual size dimorphism of nestlings is relevant to the ques-
tion of parental adjustment of the sex ratio only if there is a differential
cost to parents in raising a male versus female nestling (see Richter,
1983). It has been assumed that larger nestlings require more food from
the parents than do smaller nestlings, but we have pertinent data for
only a few species. Using doubly labeled water to measure field met-
abolic rates of nestlings, Fiala and Congdon (1983) demonstrated that
(larger) male Red-winged Blackbird nestlings display larger total assim-
ilated energy than do (smaller) female nestlings, from hatching to fledg-
ing. The difference in total assimilated energy, however, is less than
the difference in body size at fledging. Even though the difference in
energy assimilation permits the inference that parents must supply
more food to male than to female nestlings (however, see Newton, 1978,
and Newton and Marquiss, 1979), this is only an indirect measure of
reproductive cost. Furthermore, as noted by Fiala (1981b), adjustment
in either the primary or secondary sex ratios in Red-winged Blackbirds

appears to be slight, even when examined on the population scale.
An intriguing apparent exception to the above pattern is the co-
operatively breeding Red-cockaded Woodpecker (Picoides borealis), in
which Gowaty and Lennartz (1985) found male-biased sex ratios in
broods. These investigators rejected several possible explanations for
a differential cost of sons and daughters, including differential growth
or mortality and local resource competition. Local resource enhance-
ment remains a possibility. Possible associations betweeen brood sex
ratios and (1) female tenure class, and (2) presence of helpers were
examined. Tenure class permitted separation of female breeders into
those breeding for the first time in the study site and those with known
prior breeding experience at the site. Gowaty and Lennartz noted that
tenure class probably correlates with female age, breeding experience,
or kinships within breeding groups.They found that females without
prior tenure produced proportionately more sons and fewer daughters
than prior tenured females. Gowaty and Lennartz concluded that fac-
ultative variation in sex ratios is possible in Red-cockaded Woodpeck-
ers and suggested that in breeding groups in which females have sons
acting as helpers, "intersexual competition for breeding status between
mothers and sons occurs, and the tendency to overproduce daughters
(relative to other clan types) is a tactic of females that favors their own
retention within clans" (Gowaty and Lennartz, 1985).
Finally, brood reduction at the nestling stage may occur for reasons
related to differential energetic cost of raising male versus female nest-
lings (e.g., Howe, 1977b) or for other reasons (e.g., Burley, 1986). How-
ever, as discussed by Burley (1986), brood reduction is a relatively
expensive means of altering secondary sex ratios; we might therefore
expect it to be a somewhat limited phenomenon.
It is tentatively concluded that secondary sex ratios and sex ratios
at the termination of parental care in passerines generally remain close
to unity. Skewing of sex ratios that appears in adults must typically
occur after the termination of parental care.
2.3. Sex Ratios in Juveniles

We know very little about sex ratios in populations in juvenile
birds, i.e., cohorts between the ages at which parents terminate care
and sexual maturity occurs. Yet, such information is crucial; if it were
determined that skewing of sex ratios occurs during the juvenile stage,
the relative scarcity of adult female passerines need not be the result
of relatively high female PI or disparate adult mortality of the sexes

from any causes.
Potts (1969) found a male-biased sex ratio in juvenile Shags (Phal-
acrocarax aristatelis) of 1.13 (all sex ratios given as number of males
per female). A similar level of male bias occurred in every older age
class, and Potts concluded that the difference in male and female sur-
vival was not simply related to breeding. In Mute Swans (Cygnus alar),
the sex ratio becomes male biased by the age of 6 months, even though
swans do not begin to breed until at least 2 years of age, and becomes
increasingly skewed with age (Reynolds, 1972, in Yom-Tov and Olla-
son, 1976). In Great Tits, both juvenile and adult mortality rates of
females exceed those of males, leading to male-biased sex ratios in both
juveniles and adults (E. Curio, personal communication; see also Orell
and Ojanen, 1979; Regelmann and Curio, 1982). In at least five species
of North American cardueline finches, sex ratios become male-biased
prior to sexual maturity (Shreeve, 1980; Rohwer and Nolan, unpub-
lished data; S. Rohwer, personal communication). Ward (1965c) found
excesses of juvenile males over females (sex ratios = 1.2-1.7) at several
roosts of Black-faced Diochs (Q. quelea). In Starlings (Sturnus vulgaris),
the sex ratio becomes strongly male biased during the first year (Coul-
son, 1960; Charman, 1965; Feare, 1984), shifting from 0.85 to 1.67 in
one study (Coulson, 1960). The accurate timing of this dramatic shift
is confounded by the fact that first-year females breed, but first-year
males do not. Charman (1965) found that the shift in sex ratio occurred
before the first winter, prior to first breeding. However, these findings
are based on roost counts, a measure considered less than reliable by
Feare (1984). On the other hand, we lack evidence that the shift occurs
in the first breeding season (Feare, 1984).
2.4. Sex Ratios in Adults

The information on adult sex ratios in birds is in marked contrast
to the evidence that both primary and secondary sex ratios are at or
near unity, and the general scarcity of evidence one way or the other
in juveniles. There is extensive evidence that adult sex ratios are male
biased. Table I provides a compilation of this evidence; general refer-
ences, in addition to the specific studies cited in Table I, include Darwin
(1871), Mayr (1939), Bourliere (1950), Lack (1954), Brown (1969,1987)'
Trivers (1972), Welty (1975), Oring (1986), and Rohwer and Nolan (un-
published data). The studies listed in Table I are not meant to reflect
an exhaustive survey of the literature but rather suggest the general
'"
TABLE I
Male-Biased Adult Sex Ratios in Birds
Mating Adult sex Seasonal change
Species system" ratio (0' / S' )b in sex ratio e Referenced
Canvasback Duck (Aythya valisineria) M 1.2 1.1~1.4 Anderson (1984, 1985) (+)
(breeding season)
Bobwhite Quail (Colinus virginian us) M 1.1-1.2 ? Stoddard (1931) (+)
Pied Kingfisher (Ceryle rudis) C 1.7 ? Reyer (1980)
(1.7, 1.8)
Bee-eaters (5 spp.) (Merops spp.) C 1.5-2.0 ? Fry (1972)
Great Tit (Parus major) M 1.1-1.2 ? Regelmann and Curio (1986) (+)
Pygmy Nuthatch" (Sitta pygmaea) C 1.7 Norris (1958)
Brown-headed Nuthatch" (Sitta pusilla) C 1.5 ? Norris (1958)
Chiffchaff (Phylloscopus collybita) M 1.7 ? Price (1935)
Wood Warbler (Phylloscopus sibilatrix) M 1.5 ? von Treuenfels (1937)
Willow Warbler (Phylloscopus trochilus) M 1.5 ? Price (1935)
(1.2, 1.8) ~
Z
Northern Mockingbird (Mimus polyglottos) M 1.3 None Breitwisch et a1. (1986b) (+) 0
Dunnock (Prunella modularis) MX 1.3 Davies and Lundberg (1984) (+) >-
t'"
t t'"
(nonbreeding season) t:O
Superb Blue Wren (Malurus cyaneus) C 1.7 ? Rowley (1965) (+) §l
>-3
Splendid Wren (Malurus splendens) C 1.5 ? Rowley (1981) (+) ::E
European Starling (Stumus vulgaris) M 1.3 0.8~1.7 Coulson (1960) en
('J
(first year) :I:
C/l
Orange-breasted Honeyeater M 4.7 ? Mayr (1939) t'l
(Myzomela jugularis) ><
::<l
Cardinal Honeyeaterf (Myzomela M 3.1 ? Mayr (1939 >-
-3
cardinal is) 6C/l
Song Sparrow (Melospiza melodia) M 1.3 1.2~1.5 Nice (1937) (+)
>-Z
(breeding season)
0
Brown-headed Cowbird (Molothrus ater) P 1.4 Darley (1971) (+) ."
(1.3, 1.5) >-
gJ
Cassin's Finch (Carpodacus cassinii) M 4.8 None Samson (1976) (+) z
-3
American Goldfinch (Carduelis tristis) M 1.8 ? Wiseman (1975) (+) >-
r-
Gray-crowned Rosy Finch (Leucosticte M 4.5 ? Shreeve (1980) (+)
Z
atrata) <:
t'l
Red Bishop (Euplectes orix) P 1.1 Craig and Manson (1979) (+) C/l
t -3
(1.1, 1.2) (breeding season) :::::
t'l
Red-shouldered Widow (Euplectes P 1.2 t Craig and Manson (1979) (+) Z
-3
axillaris) (breeding season)
House Sparrow (Passer domesticus) M 1.1 R. F. Johnston (personal
communication) (+)
Black-faced Dioch (Quelea quelea) M 1.8 1.~4.2 Ward (1965a, b, c) (+)
(nonbreeding season)
OM, monogamous; C, cooperative breeder; P, polygynous; MX, mixed [see Davies and Lundberg, 1984); for sex ratios of polyandrous species, see Gring [1986).
bSingle number is mean sex ratio if study lasted more than 1 year; a range of values is that given by author of study; two numbers in parentheses are values
for two populations.
'?, unknown; i, increase; 1, decrease; none, there is evidence of no change seasonally; statement in parentheses indicates when change occurs if this
known.
d +, multiyear study; no symbol, single-year study.
'Information from museum specimens.
fInformation based on populations from seven islands.
<.D
nature of male-biased adult sex ratios in birds by the taxonomic di-

versity displayed.
Documentation of adult sex ratios is complicated by particular
mating systems and the presence of floaters. Together, these factors
make it difficult to distinguish between an actual tertiary sex ratio (that
of all sexually mature adults) and the operational sex ratio (Emlen,
1976; Emlen and Gring, 1977). This problem becomes particularly acute
for polygynous species, in which some males are forced into behav-
iorally inconspicuous roles as floaters, producing the appearance of a
strongly female-biased sex ratio when in fact, the actual tertiary sex
ratio may be close to unity. This problem is much less severe in mo-
nogamous systems, although floaters certainly exist in many such spe-
cies (Brown, 1969; S. Smith, 1978). The only method that ensures an
accurate count of both males and females would involve removal of
territorial individuals or pairs and detection of new individuals settling
on the partially or completely vacant territories. The findings of Stewart
and Aldrich (1951) and Hensley and Cope (1951) are well known in
this regard and should serve as a caution to investigators interested in
determining the actual sex ratios in populations of adult birds.
3. MORTALITY PATTERNS
We should expect to observe different mortality schedules for the

sexes in a variety of species of birds and other animals. Males and
females differ morphologically, physiologically, behaviorally, and fre-
quently genetically (Mayr, 1939; Trivers, 1972; Glucksman, 1974; Mur-
ray, 1984; VelIe, 1987; Breitwisch and Hudak, 1989). Further, there is
no evolutionary mechanism to return skewed sex ratios to unity if they
depart from unity after the termination of parental care (Fisher, 1958;
Charnov, 1982).
This section discusses the evidence for differential mortality sched-
ules for the sexes, seeking common patterns among species. Because
the evidence so far discussed has shown that sex ratios become male
biased sometime after the termination of parental care, the emphasis
is on juvenile and adult mortality patterns. First, juvenile mortality,
i.e., mortality between the termination of parental care and the age of
sexual maturity is discussed. Adult mortality patterns, distinguishing
between breeding and nonbreeding seasons are then discussed, asking
to what extent deaths in the two seasons of the annual cycle are func-
tionally isolated.
Four ways in which male and female birds are different may con-
tribute to differential mortality between the sexes. These four differ-

ences are (1) natal dispersal, (2) body size, (3) sex chromosomes, and
(4) reproductively related behavior. The first of these-natal dispersal-
is the only one restricted to consideration of juvenile biology. The last-
reproductively related behavior-clearly is restricted to sexually ma-
ture adults. The other two-body size and sex chromosomes-should
act in both juveniles and adults, although we might expect most neg-
ative effects of heterogamy to be displayed in young individuals, in-
cluding embryos and nestlings (Landauer, 1967). The first three of these
are discussed in turn, followed by a summary of their effects on juvenile
and adult birds before proceeding to a discussion of PI.
The discussion of PI as a source of mortality is separated because
(1) this is the only hypothesized source of mortality that has been widely
assumed to act disproportionately and significantly on females in mo-
nogamous passerines, (2) there are substantial reasons to question our
assumption of high female PI, and (3) PI patterns may be viewed par-
tially as the result of other sources of mortality and the consequently
skewed sex ratios rather than as the primary cause of female scarcity.
3.1. Juvenile Mortality

What are the primary causes of mortality in juvenile birds? For
many years, it has been known that juveniles newly independent from
parental care are relatively inept at foraging (Breitwisch et 01., 1987,
and references cited therein). It has been inferred that this leads to
differential mortality of juveniles through increased probabilities of
starvation and perhaps predation due to the increased foraging time
required to meet basic nutritional needs (Lack, 1954, 1966; Welty, 1975).
Subordinate status relative to behaviorally dominant adults can inten-
sify these problems (Gauthreaux, 1978; Martin, 1987). In addition, for
migrating species, there is some evidence that mortality related to mi-
gration is greater for juveniles than for adults (Johnson, 1973; Greenberg,
1980; Gauthreaux, 1982).
There is no doubt that the juvenile stage is a period of heavy mor-
tality for birds. What has not been asked is whether there are reasons
to suspect that males and females are differentially susceptible to these
sources of juvenile mortality. In fact, very few investigators have dis-
cussed possible sex differences in juvenile mortality. Trivers (1972)
allowed for sex differences in juvenile mortality in his model of dif-
ferential mortality between the sexes, but he discussed only those com-
ponents of mortality borne as a cost of acquiring attributes beneficial
in achieving reproductive success. Such attributes presumably would
include weaponry used by males in intra sexual competition for mates

or nonbreeding experiences of either sex beneficial to breeding.
3.1.1. Natal Dispersal and Mortality

Sex differences in juvenile mortality rates in birds may result from
different natal dispersal distances in juvenile males and females. It is
common for female birds (both passerines and nonpasserines) to undergo
longer distance natal dispersal than males (reviewed by Greenwood,
1980; Gauthreaux, 1978, 1982; Greenwood and Harvey, 1982; Shields,
1982). For Great Tits in Wytham Woods, this difference is on the order
of 200-300 m (Greenwood et al., 1979). For Tits in southern Sweden,
80% of males were found within 510 m and 80% of females within 900
m of their place of birth in July of their first year; females dispersed
farther than males for known dispersers (Dhondt and Huble, 1968;
Dhondt, 1979). For Florida Scrub Jays (Aphelocoma coerulescens coe-
rulescens), the mean difference in natal dispersal is nearly 1 km (male
mean distance: 304 m; female mean distance: 1163 m) (Woolfenden
and Fitzpatrick, 1984); this difference is typical of communal breeding
species (Greenwood and Harvey, 1982; Brown, 1987; Koenig and Mumme,
1987).
Dispersal includes a cost not borne by individuals remaining on
or near the natal territory (Hamilton and May, 1977; Wiley and Raben-
old, 1984; Liberg and von Schantz, 1985; Brown, 1987; Eden, 1987;
however, see Dhondt, 1979). The prediction of differential mortality
associated with different distances of natal dispersal originated from
studies of small mammals (Lidicker, 1975; Dunford, 1977). It is still
largely unknown, however, whether such differential mortality exists
in birds. Exceptional cases are Red Grouse, Lagopus lagopus scoticus,
and Florida Scrub Jays. In both, young females disperse farther than
young males and suffer greater mortality in the period between hatching
and first breeding (Jenkins et al., 1967; Woolfenden and Fitzpatrick,
1984). Furthermore, it has been shown that young male Blackbirds
(Turdus merula) dispersing long distances risk a higher probability of
death during their first 2 years than young males settling close to their
natal territories (Greenwood and Harvey, 1976).
In adults, following nesting failure, females typically disperse far-
ther than males (Nice, 1937; Thompson and Nolan, 1973; Gauthreaux,
1978; Nolan, 1978; Greenwood, 1980; Greenwood and Harvey, 1982;
Rohwer, 1986), even though this may involve a cost in time to renesting
(Wunderle, 1984). Thus, there may be greater dispersal-related mortal-
ity in adult as well as in juvenile females.
If females suffer a cost in farther natal dispersal, there should be

compensating gains from doing so (however, see Gauthreaux, 1978).
Possible benefits to females have been suggested by Greenwood (1980)
and Liberg and von Schantz (1985). It remains notable, however, that
the assumption of increased cost with dispersal distance has not yet
been generally verified among species.
There is a reversed patten of dispersal in waterfowl, with males
dispersing farther than females (Greenwood and Harvey, 1982; Green-
wood, 1983). Do male-biased sex ratios in waterfowl refute the hy-
pothesis of a significant cost to dispersal? There is a confounding factor,
in that female waterfowl store substantial nutrients for egg formation,
unlike most passerines (see Section 4.2.1). Thus, PI patterns for water-
fowl may be quite different from those of monogamous passerines, and
costs of high PI may overwhelm costs of dispersal on the population
sex ratio.
3.1.2. Migration and Mortality

Migration can result in heavy mortality (Welty, 1975). Where there
is evidence of differential migration between age and sex classes, the
general pattern is one in which juveniles migrate farther than adults
and within age classes, females farther than males (reviewed by Gauth-
reaux, 1978, 1982). In some cases, a fraction of the adult population
(predominantly males) remains in the breeding range on or near their
breeding area as year-round residents, while other members of the pop-
ulation migrate varying distances (Lack, 1968b; reviewed by Ketterson
and Nolan, 1983). Another variation on this pattern manifests itself not
in distance but rather in habitat quality: adults overwinter in habitats
of better quality than do juveniles, and males in better habitats than
females (Gautheraux, 1978, 1982).
Intersexual differences in distance of migration within populations
are like that in natal dispersal. Indeed, Gauthreaux (1978) proposed
that behavioral dominance is the mechanism accounting for the similar
pattern. Males are dominant to females, and adults are dominant to
juveniles. Subordinates move farther and/or into poorer habitats as a
result of these behavioral interactions.
Although we lack complete understanding of such differential or
partial migration, it is a phenomenon which may be common to many
temperate zone breeding birds. In White-crowned Sparrows (Zonotri-
chia leucophrys gambelii) and Dark-eyed Juncos (Junco hyemalis hye-
malis), for example, the differences in distance of migration between
males and females are dramatic, with females migrating much farther
than males. In wintering White-crowned Sparrows, the sex ratio in a

Washington population was 4.0, while the sex ratio in a southern Ar-
izona population was 0.25, with a clear latitudinal cline (King et a1.,
1965). In Dark-eyed Juncos, winter population sex ratios in northeastern
u.S. samples were 4.0, decreasing latitudinally to 0.4 in southeastern
u.S. populations (Ketterson and Nolan, 1983)
Ketterson and Nolan (1976) argued that there is a correlation be-
tween distance of migration and risk of mortality, independent of sex.
If true, female juncos, for example, would suffer a greater probability
of dying in migration than males, which could act to skew the juvenile
and adult sex ratios. Ketterson and Nolan propose that higher female
mortality due to migration is offset by higher male mortality due to
overwintering in more northern latitudes (Ketterson and Nolan, 1982;
see also Gauthreaux, 1982), and the result is a tertiary sex ratio of unity
that remains so year after year in adult cohorts. However, the reported
data purporting unity in adult Junco sex ratios are scanty.
The critical correlate of differential migration is assumed to be
differential cost or probability of mortality in migration. If this occurs,
juveniles should, in general, suffer higher mortality than adults and,
within age classes, females should suffer higher mortality than males.
There is no reason to suspect a compensatory winter mortality of res-
idents in such species that would necessarily result in sex ratios of
unity during subsequent breeding seasons. It is possible that tertiary
sex ratios in migratory populations become skewed as a result of dis-
parate mortality from migratory movements.
3.2. Age-Independent Mortality

3.2.1. Sexual Size Dimorphism and Mortality
Body size can influence survival in both juvenile and adult birds.
In many birds, including monogamous species, males are slightly larger
than females (Selander, 1966, 1972); these size differences develop in
nestlings (Howe, 1977a,b; Fiala, 1981a,b). Even small differences in
body size of birds-typically 5-10% by weight in monogamous pas-
serines- can influence probability of survival, especially under harsh
conditions, with smaller females suffering higher mortality than larger
males (Ward, 1965c; Boag and Grant, 1981, 1984; Schluter and Smith,
1986).
Boag and Grant (1981) documented a skewing of the tertiary sex
ratio in Darwin's Medium Ground Finch (Geospiza fortis) on Daphne
Major, Galapagos Islands, during the 2-year period between June 1976
and March 1978, with a change from 1.0 to ~6.0. Severe drought con-
ditions during this period led to an increase in the relative proportion
of large hard seeds and a decline in small soft seeds. Male G. fortis on
Daphne Major are approximately 4% larger than females in linear mea-
surements, and large males apparently survived the drought better than
small females due to their ability to handle large seeds with their heavy
bills. Similar patterns of mortality and skewing of the sex ratio occurred
in two subsequent drought periods (Boag and Grant, 1984; Price et aI.,
1984).
The degree of sexual dimorphism in House Sparrows (Passer do-
mesticus) was found to be increased for both juveniles and adults during
a harsh winter in eastern Kansas Oohnston and Fleischer, 1981; Fleischer
and Johnston, 1982). Among males, relatively large individuals and,
among females, relatively small individuals were favored, and the form
of selection (on body size and shape) was different for the sexes. Male
and female sparrows in Kansas are monomorphic in bill parameters,
so selection must have favored other aspects of body morphology. It
appeared that the ratio of size of body core to length of appendages was
the aspect of shape acted on and altered. Johnston and Fleischer did
not address the question of sex ratio skewing as a result of these mor-
tality patterns, so we do not know to what degree such harsh selection
may also act to alter this.
In some species, dominance hierarchies (mediated by body size)
for access to food can be a mechanism that skews sex ratios in either
juveniles or adults (Yom-Tov and OHason, 1976; De Laet, 1985). For
example, nonbreeding season mortality is higher in female than male
Willow Tits (Parus montanus) and Crested Tits (P. cristatus), and this
difference appears due to starvation mediated by a size-related domi-
nance hierarchy. This component of mortality may not be a cost of
breeding paid in the subsequent nonbreeding season. Physiological
"debts" are paid with little delay, due to the rapid turnover of energy
in passerines (Ricklefs, 1977; Alerstam and H6gstedt, 1984; Ekman and
Askenmo, 1986; J. Ekman, personal communication).
Small body size may still be viewed, however, as a cost of repro-
duction to females, although not in the usual sense (W. A. Searcy,
personal communication). If females are smaller than males due to a
breeding advantage over larger females (Downhower, 1978), then a higher
probability of mortality in the nonbreeding season related to small body
size might be a cost associated with this benefit.
Sexual size dimorphism in monogamous species is maintained by
the combined forces of natural (= survival) and sexual selection acting
differently on the sexes (Selander, 1972; Downhower, 1978; Searcy,
1979a; Price, 1984; Jehl and Murray, 1986). Both natural and sexual
selection should usually favor males of relatively large body size (how-
ever, see Petrie, 1983a,b; Mueller and Meyer, 1985; Jehl and Murray
1986). Females will not be subject to sexual selection to the same degree,
and female body size should largely reflect aspects of natural selection;
i.e., female size is an optimum body size for the population, and sexual
selection pushes males away from this optimum (Price, 1984). Rela-
tively large females may better survive harsh nonbreeding season con-
ditions (e.g., freezing temperatures, drought conditions, or food short-
ages) because they can store more nutrient reserves than smaller females,
while smaller females can more quickly initiate reproduction with rapid
increases in availability of nutrient resources required for breeding
(Downhower, 1978; Perrins, 1979; Murphy, 1986). For males, there
should be no size-related difference in the time necessary for physio-
logical response to increasing nutrient resources because sperm pro-
duction is essentially independent of nutritional reserves (King, 1973).
Smaller body size may act synergistically with inexperience and
with farther natal dispersal in juvenile females to produce higher mor-
tality rates than in juvenile males. The result would then be a scarcity
of young females entering the breeding population the next season.
3.2.2. Heterogamy and Mortality

As the heterogametic sex, female birds may be subject to higher
embryonic and nestling mortality than males. Higher embryonic mor-
tality in females occurs in that species of bird providing the largest data
sets, the Domestic Chicken (Landauer, 1967). Lower female survival
would be analogous to lower embryonic and neonatal survival in het-
erogametic male mammals (see Myers, 1978; McMillen, 1979). Al-
though heterogamy (the chromosomal hypothesis) was rejected by Triv-
ers as an explanation for differential mortality of the sexes, I wish to
resurrect this hypothesis as a theoretical possibility that warrants fur-
ther study. We lack the data necessary to evaluate the influence of
heterogamy on mortality in organisms (Bull, 1983; B. Charlesworth,
personal communication).
Trivers (1972) rejected the chromosomal hypothesis as an expla-
nation for differential mortality of the sexes for three reasons: (1) in
several species of mammals, castrated males outsurvive intact control
groups, (2) the observed magnitude of mortality differences between
the sexes far exceeds theoretical predictions, and (3) patterns of dif-
ferential mortality across species are not those predicted by known sex-
determining mechanisms. The first two should not be taken as causes
for rejection of the chromosomal hypothesis (see Myers, 1978). Heter-

ogamy may account for a significant portion of differential mortality,
with these points still valid.
The theoretical predictions of mortality levels from heterogamy
were based on a model derived from mammalian data. There is little
reason, however, to accept uncritically an argument from mammals
extended to any other organism (e.g., birds) in which heterogamy de-
termines sex (B. Charlesworth, pers. comm.). The relative cost of ex-
posed recessive deleterious alleles in the heterogametic sex may vary
widely within and among different major taxa in which sex is so de-
termined (Bull, 1983).
Differential mortality patterns of the sexes among species were
believed not to agree with predictions based on sex-determining mech-
anisms. For instance, Trivers (1972) states "Female birds are hetero-
gametic but suffer higher mortality only in monogamous species." I
contend that this is simply an assertion; we do not yet possess the data
necessary to make such a claim. The evidence we do possess (vide
supra) suggests no reason to believe that monogamous birds differ from
other birds in this regard.
Heterogamy cannot in isolation account for the magnitude of male-
biased sex ratios in birds. Although it is difficult to offer theoretical
predictions of the importance of heterogamy in birds, as much as several
percent greater female mortality may be due to sex chromosomes
(B. Charlesworth, personal communication).
3.3. Conclusions
It is plausible that adult sex ratios in monogamous birds become
male biased via some combination of differences in natal dispersal,
migration, body size, and sex chromosomes. The result of such a limited
supply of females clearly would be male competition for access to
females. Theoretically, the effects of a sex ratio initially skewed in
juveniles, for example, can thus precede Trivers's (1972) proposed ef-
fects of differential PI between the sexes in determining which sex is
a limiting resource for the other.
We possess only a rudimentary knowledge of mortality patterns in
wild birds (Dobson, 1987). Of primary consideration in future inves-
tigations of mortality should be the questions of when and how indi-
viduals die and, in particular, the interseasonal influence of condition
of health (R0skaft, 1985). The less this influence, the more critical the
question of timing of mortality. Although it has been assumed that the
interseasonal influence is substantial, physiologists are questioning this
assumption, especially for passerines (e.g., Ricklefs, 1977; Walsberg,

1983a,b; Alerstam and Hagstedt, 1984). One of the greatest challenges
to avian physiological ecologists is to determine the degree of functional
isolation versus dependence in the health of birds in the breeding and
nonbreeding seasons. The implications of this (in)dependence extend
to the evolution of PI patterns between the sexes and, quite probably,
to our complete understanding of the prevalence of monogamy in this
group.
4. MALE AND FEMALE PARENTAL INVESTMENT
One might expect that, 15 years after Trivers's provocative paper,

we have a large array of species for which the components of PI have
been assessed for the sexes. This is not the case. To my knowledge, for
no species of biparental, monogamous bird have all the major com-
ponents of PI been assessed. Perhaps the best studied is the Northern
Mockingbird, although its treatment is incomplete. Others include the
Canvasback Duck (Aythya valisineria), American Oystercatcher (Hae-
matopus palliatus), and Stonechat (Saxicola torquata). For the other-
wise well-studied Great Tit, no one has compiled the various data sets
on parental care to compare PI by the sexes.
Furthermore, investigators are still undecided on which compo-
nents of behavior should be included in PI and which excluded. Cer-
tainly, at one extreme, all aspects of behavior in an individual's life
prior to and during reproduction could be included. Only slightly less
extreme is the view that everything an individual does in the breeding
season could be included (e.g., Nol, 1985). Clearly, for utilitarian pur-
poses, this concept must be restricted. Low (1978) divided the repro-
ductive effort for any breeding attempt into mating effort and parental
effort. Parental effort equals the sum of PI in each offspring, taking into
account that some PI is nonshareable (Wittenberger, 1981). My use of
the term PI therefore coincides with Low's use of parental effort (here,
for a clutch or brood of offspring).
Territorial behavior presents a problem to the investigator of PI.
Some authors claim this as a part of PI (e.g., Trivers, 1972; Gladstone,
1979, Howe, 1979; Nol, 1985), while others exclude it (e.g., Witten-
berger, 1981; Breitwisch et a1., 1986b). Defense of territory may, instead,
qualify as PI depending on its context. On the one hand, there are birds
in which unmated males hold territories, at least during part of the
breeding season. Certainly, it appears unreasonable to include this be-
havior within PI. The particular unmated male may remain unmated
his entire life, yet, if his territorial defense were included in PI, he
could find himself in the peculiar position of having expended con-
siderable time and energy, and perhaps taken some risk, as PI. However,
what if territorial behavior by a male or pair benefits their offspring by
providing defended foraging areas in which food for the offspring is
gathered? Furthermore, what if such territorial defense by a male or
pair is stronger than by an unmated male or lasts longer in the breeding
season? What if a pair decreases territorial defense immediately after
their nestlings or fledglings are preyed upon? But, what if territorial
defense in a species is only defense of a nest hole against predators?
A solution to the problem of territorial defense may be to exclude
from PI any territorial defense before eggs are produced. Beyond that
time, subsequent territorial behavior would qualify as PI. A further
refinement may be to include only that portion of post-egg production
territorial defense that exceeds the level extended by unmated males
at that time in the season. Clearly, students of PI need to discuss further
the problem of territorial defense and PI.
It is worth mentioning here that some authors appear to have mis-
interpreted Trivers's definition of PI to refer only to a reduction in the
parent's ability to invest in future offspring. Trivers, however, did not
restrict use of the term "other offspring" to future offspring only; rather,
this can also refer to current offspring. Thus, theoretically PI can limit
clutch size in species in which female investment in individual gametes
is substantial. In birds, the female's provisioning of relatively large
gametes is clearly different from many nonavian species in which egg
provisioning is slight, and clutches are, in some cases, huge. This does
not mean that optimal clutch sizes in birds are set by physiological
constraints on egg production (see Winkler and Walters, 1983; Murphy
and Haukioja, 1986), only that there are limits to the number of large
eggs a female can produce over a short period of time.
Trivers (1972) suggested that female birds in monogamous species
expend somewhat higher levels of PI than do males. Numerous inves-
tigators in subsequent studies on components of parental care in mo-
nogamous birds apparently have accepted this suggestion even in the
general absence of data. This acceptance may well reflect our mam-
malian bias. The cost of reproduction to female mammals is well known
(see, e.g., Pond, 1977; Clutton-Brock et aI., 1982), as is the limited role
of male mammals in parental care. But oviparous birds potentially are
very different from viviparous, lactating mammals, and the prevalence
of biparental care and monogamy are two primary distinctions (Wit-
tenberger and Tilson, 1980). We need to test the assumption of high
female PI in birds.
4.1. The Problem of Currency

A critical difficulty with PI theory is that of commensuration of
investments (Walsberg, 1983a,b; Knapton, 1984; Mock, 1985). How can
we combine energy and time investment along with a risk factor in
order to assess male and female PI and then compare the sexes? This
dilemma has been termed the "problem of currency" by Knapton (1984),
who provided a hypothetical example of a bird displaying division of
labor by the sexes in parental care such that it would be most difficult
to compare the sexes. My outlook is not as bleak as Knapton's. I believe
we will be able to assess relative PI in some species with biparental
care, although other species displaying a division in care similar to
Knapton's scenario indeed may thwart our efforts.
Acknowledging these difficulties, investigators typically measure
time and energy expended and may attempt to assess risk involved in
several behavioral components of PI. This is presumably what birds do
in maximizing lifetime reproductive success. They have only time and
energy available to them and must act as if they weigh relative risk of
injury or death in spending time and energy on aspects of parental care.
Before Trivers, Kendeigh (1952) stated that feeding rates to nest-
lings (a primary component of parental care) appeared to be more or
less equal between mates in many monogamous species. In a broad
review of male parental care in North American passerines, Verner and,
Willson (1969) stated that males in a majority of monogamous species
for which data were available assist with nest construction and egg
incubation, and virtually all feed nestlings and fledglings. For ade-
quately reported species, they note that males feed incubating females
in most. Perhaps just as important as these conclusions, however, was
their bemoaning of the inadequacy of our general information on the
prevalence of these aspects of male parental care. Although providing
a wealth of information on parental care in many species of birds,
Skutch (1976) attempted little in the way of summarizing this infor-
mation. In agreement with Trivers, Emlen and Gring (1977) suggested
disparate PI in monogamous birds, with females investing more than
males. However, they neglected aspects of PI subsequently demon-
strated to be of importance, such as defense of offspring (Andersson et
aI., 1980; Curio, 1980; Regelmann and Curio, 1986; Breitwisch, 1988)
and care of fledglings 0. Smith, 1978; Zaias and Breitwisch, 1988).
Searcy and Yasukawa (1981) assumed that higher mortality of adult
females than males in some species of blackbirds (Icteridae) was due
to greater PI by females, but they did not consider other possible sources
of female mortality. My contention is that we do not possess sufficient
data to support a general assumption that females in monogamous spe-

cies of birds expend greater PI than males (Reznick, 1985).
4.2. Female Parental Investment

Several arguments mitigate against the assumption that female PI
is necessarily high in monogamous birds.
4.2.1. Egg Production

Egg production by female birds has long been argued to be ener-
getically expensive (e.g., Jones and Ward, 1976). This view is changing
(Gladstone, 1979; Murray, 1979, 1985a; Erckmann, 1983; however, see
Martin, 1987). The energetic cost of eggs to females varies among species
but is moderately small for passerines hatching altricial young (Perrins,
1970; Ricklefs. 1974; Ar and Yom-Tov, 1978; Walsberg 1983a). Walsberg
(l983a), for example, calculated for five small «25g) passerines that
the energetic content of the clutch is equivalent to only ~2% of the
female's total energy expenditure during a single reproductive event.
Peak energy requirements of egg production have been estimated as
~45% of total basal metabolic rate in passerines (Ricklefs, 1974). These
requirements are much greater in some nonpasserines hatching pre-
cocial young, especially waterfowl that store energy for egg production
even prior to the breeding season (Ricklefs, 1974).
There are other possible nutritional costs to egg production. The
most likely is that of calcium deposition. A hen laying 250 eggs per
year secretes into shells ~20 times its body content of calcium (Mueller,
1976). Calcium ion must be extracted continuously from blood because
shell glands store little calcium. There are both increased rates of in-
testinal absorption and mobilization from medullary bone during laying
(Mueller 1976). Medullary bone (unique to female birds) forms 1-2
weeks before egg-laying in hens. This bone is extremely labile, being
formed and resorbed at rates far in excess of other forms of bone (Simkiss,
1975). Females of some birds display a "calcium appetite" during re-
production (Hughes and Wood-Gush, 1971; Simkiss, 1975; Fogden and
Fogden, 1979).
Polyandrous birds can lay a large number of clutches within a
season, and these clutches represent an impressive total egg mass. The
total calcium content of the several clutches of eggs produced by poly-
androus Spotted Sandpipers (Actitis macularia) in a single breeding
season is several times the total calcium content of a female sandpiper's
body tissues (Maxson and Gring, 1980). This may suggest that calcium
deposition is potentially costly, requiring elevated foraging activity and/

or the drawing of calcium from storage in medullary bone (Maxson and
Dring, 1980). Alternatively, one may view the prodigious egg-laying
abilities of hens and polyandrous birds (after all, they do it) as evidence
suggesting a relatively low cost of calcium deposition for monogamous
passerines and nonpasserines hatching altricial young in which females
produce a proportionately smaller egg mass per season.
Finally, there are recent suggestions that the energetic cost of male
ejaculate may be greater than previously assumed (Gladstone, 1979;
Dewsbury, 1982), decreasing the supposed disparity between the sexes
in gamete costs. This possibility should be investigated in birds with
social systems favoring sperm competition (McKinney et a1., 1984).
4.2.2. Weight Loss

Investigators have also used data on weight losses by breeding
females as a measure of reproductive effort (e.g., Howe, 1979; De Steven,
1980; Sasvari, 1986). Caution is necessary, however, in assessing these
weight data; ovary regression is likely to be responsible for much of
the decrease in weight of female birds as the breeding season progresses
(Ricklefs, 1974; Ricklefs and Hussell, 1984). We do not know, in general,
whether female physiological vulnerability to stressful environmental
conditions or energy demands increases significantly with seasonal
weight loss (Murphy and Haukioja, 1986). Moreover, weight loss may
be an inadequate measure of an individuals's condition (Johnson et a1.,
1985). Furthermore, it was recently argued that female weight loss may
be adaptive in terms of decreasing power consumption in flights de-
livering food to young, hence may not even reflect a reproductive cost
(Freed, 1981; Norberg, 1981; Murphy and Haukioja, 1986).
4.2.3. Timing of Investment

Incubation and brooding are not expensive energetically for most
birds (King, 1974; Walsberg, 1983a,b). In fact, an incubating or brooding
female may conserve energy relative to her mate's expenditures in var-
ious activities (e.g., Biedenweg, 1983; R0skaft, 1983). However, restric-
tion on time available for foraging by an incubating female is large
enough in some species to suggest an effect on reproductive output
(Walsberg, 1983a). Walsberg argued that only energy expenditures later
in a nesting event (caring for nestlings or fledglings) may truly represent
PI, i.e., energy unavailable for a subsequent nesting event at that time
(see McGillivray, 1983). During the breeding season, female birds, es-
pecially passerines, simply do not store energy longer than a period on

the order of a day or two.
4.2.4. Fecundity and Survival

If the physiological costs of high PI in females are great, we might
expect an inverse relationship between fecundity and survival in fe-
males within a population. Yet, in only a limited number of cases have
investigators found such a relationship. For instance, in a recent review
of studies of reproductive costs in a variety of organisms, Reznick (1985)
found that only 22 of 33 correlational studies demonstrated such a
tradeoff between fecundity and survival. Only two of these studies were
on birds, and only one of these found the negative correlation expected
as a reflection of reproductive cost (Bryant, 1979; see also Ekman and
Askenmo, 1986). Reznick concluded that the other studies on birds
purporting to demonstrate reproductive cost were not sufficiently rig-
orous to substantiate that claim. Murphy and Haukioja (1986), in re-
viewing the question of reproductive cost to birds, concluded that "Al-
though it is clear that at some hypothetical rates of reproduction there
are survival costs to parents, reproduction may be practically noncostly
at the range of realized clutch sizes for most nidicolous birds." In effect,
there may be threshold clutch and brood sizes for species or populations
of females, below which females generally pay no reproductive cost
(Tuomi et aI., 1983).
A recent study by Rockwell et a1. (1987) on Snow Geese (Anser c.
caeruiescens) amassed very large samples over a 12 year period. They
showed that return rates of females (used as a measure of adult female
survival) did not depend on reproductive output for clutch sizes varying
between one to seven eggs. Fecundity measures were number of eggs
laid, number of goslings leaving the nest, and brood size at fledging. A
significant effect of clutch size at hatching on return rates was accounted
for by a very low return rate of parents laying single-egg clutches, but
these predominantly were young inexperienced birds. Rockwell et a1.
(1987) concluded that female (and male) survival was independent of
reproductive performance (see also Loman, 1980; Lessels, 1986).
Others (e.g., Nur, 1984) claim an inverse relationship between fe-
cundity and mortality by equating female disappearance with death.
Disappearance clearly is an inadequate measure of mortality in popu-
lations open to migration. Female birds always retain the option of
dispersing. Manipulative experiments, such as Nur's (1984) with Blue
Tits (Parus caeruIeus), in which brood sizes are artificially increased
may lead to female emigration as a response to nest disturbance.
An argument sometimes made to explain the lack of a relationship

between fecundity and survival is that females of different quality ad-
just their fecundity to match their quality (Hagstedt, 1981; Smith, 1981).
If true, the probability of death will be similar among females regardless
of brood size (Reznick, 1985). This possibility warrants investigation.
4.2.5. Vulnerability of Nesting Females

It has been assumed that incubating or brooding females have greater
probabilities of being preyed upon, especially by nocturnal predators,
than roosting males. In this way, female PI is increased relative to male
PI. However, there are various behavioral responses to predators by
incubating and brooding birds that must reduce their vulnerability (Drent,
1973). We currently possess limited data to examine the claim of greater
vulnerability of nesting females; much of the purported evidence is in
the form of female disappearance.
4.2.6. Female Disappearance

Most avian biologists studying questions of PI and reproductive
effort and cost in the field study populations open to migration of
individuals. It is therefore difficult to know the fate of disappearing
birds. As is argued here, the two explanations of female disappear-
ance-death or abandonment-reflect markedly different situations.
Death by predation or by overtaxing physiological functions in caring
for offspring is true PI. However, abandonment may have nothing to
do with the individual's PI, except to indicate that the abandoning bird
will invest later in offspring produced with a different mate. For ex-
ample, female abandonment may sometimes follow nesting failure be-
cause of some deficiency on the part of the mate, e.g., inadequate PI
(Diamond, 1987). In such cases, female disappearance (perhaps mis-
takenly scored as death by the investigator) may reflect a typically high
level of male PI, or at least male investment in crucial components of
parental care (Petrie, 1983a), i.e., precisely the opposite interpretation
from female death. A disappearing female, then, is simply obeying a
behavioral rule to disperse if her first mate has not performed as ex-
pected. It is known, for instance, that divorce in birds frequently follows
nesting failure (Rowley, 1983).
It is instructive to consider data on death and disappearance of
females from two well-known long-term studies, Nice's (1937) study
of the Song Sparrow and Nolan's (1978) of the Prairie Warbler (Den-
droica discolor). If reliable data exist on the frequency of female death
in the breeding season, we might expect to find these in such long-term

studies. Although she found higher rates of female than of male dis-
appearance during the breeding season, Nice suspected that the dis-
parity may have been due to female dispersal rather than mortality; as
females disappeared, new young females entered the study area. Nolan
found no difference in adult mortality of the sexes during the breeding
season, and a tertiary sex ratio of unity. These results thus do not
support the assumption of high female PI, i.e., high cost of breeding,
relative to male cost.
A comparison of two studies reflects, I believe, our bias with respect
to fates of disappearing females versus males. Askenmo (1979) reported
that male Pied Flycatchers (Ficedula hypoleuca) returned the following
season in lower proportion from pairs caring for artificially enlarged
broods than from control pairs. This was interpreted as male death
until Hbgstedt (1981) made a persuasive argument that experimental
males had more likely abandoned their territories and settled elsewhere
as a response to the manipulation. By contrast, Nur (1984) has argued
that female Blue Tits (Parus caeruleus) that disappeared after caring
for artificially enlarged broods had died (high parental effort). For some
reason, we seem more willing to accept death to abandonment in this
interpretation. But, is it not just as likely that the female tits have
abandoned their territories in response to Nur's manipulation? Fur-
thermore, might not more females leave when faced with a larger per-
turbation (i.e., a greater artificially increased clutch size), just as found
by Nur (1984)? Reid (1987) also has assumed that female Glaucous-
winged Gulls (Larus glaucescens) that disappeared from manipulated
clutches had died, and he based his discussion of reproductive costs
on this assumption. The question of abandonment in such experiments
is of real importance; it is known that female birds under natural con-
ditions are typically less philopatric than males (Gauthreaux, 1982). In
the rush to perform manipulative experiments in the field, we need to
reaffirm our recognition that simple disappearance of an individual in
a population open to migration is clearly a large step removed from
knowledge of the fate of the individual.
4.3. Male Parental Investment

Whereas several factors that potentially mitigate against an argu-
ment for high female PI have been discussed, there appear to be several
factors that enter into male PI but have been little discussed. These, I
believe, argue further for a reassessment of male PI. Male birds engage
in several aspects of behavior that may be important components of PI.
These include defense of offspring against predators, courtship and/or

incubation feeding of their mates, and protection of their mates. The
latter two components are indirect parental care but must nonetheless
be included in an assessment of total male PI.
4.3.1. Brood Defense

Regelmann and Curio (1986) noted the generality of the finding
that male birds tend to defend their broods against predators more
strongly than do females. It is clear that many instances of such defense
include a risk to the parent bird. Curio and Regelmann (1986) cite
extensive evidence for the assumption that brood defense can be dan-
gerous. Breitwisch (1988) recorded that the large majority of attacks on
potential predators (= human intruders) near nests by Northern Mock-
ingbirds were launched from behind the predator. The prevalence and
intensity of (especially male) brood defense argues for its necessary
inclusion as a significant component of PI.
4.3.2. Courtship and Incubation Feeding

In a variey of species, males feed their mates during either courtship
or incubation, or both, and this provides some portion or all of a female's
nutritional needs at those times (Royama, 1966a; Verner and Willson,
1969; Krebs, 1970; Perrins, 1970; Nisbet, 1973; Kemp, 1978; Ligon,
1978; Fogden and Fogden, 1979; Newton et aI., 1983; R0skaft, 1983;
Lyon and Montgomerie, 1985; Lifjeld and Slagsvold, 1986, Beissinger,
1987). This activity requires time and energy spent by males and ex-
poses males to some risk of predation accompanying foraging. It may
be viewed as a form of indirect PI.
Lyon and Montgomerie (1985) recently experimentally investigated
incubation feeding in Snow Buntings (Plectrophenax nivalis), a species
in which males typically provide some portion of the female's food
during incubation. They widowed females either early or late in in-
cubation and demonstrated higher egg loss in early widowed birds, as
these females spent more time off the nest, foraging, than late widows
or control females. Because the pair benefits in immediate reproductive
success from incubation feeding, Lyon and Montgomerie viewed this
as a form of indirect parental care by males. These workers concluded
that incubation feeding is not a case of female manipulation of the
male, but it should be noted that they use this term in a restricted sense.
Incubation feeding may still be an aspect of parental care demanded
by females, and we assume that there is potentially some cost to the
SEX RA nos AND PARENTAL INVESTMENT 27
male in the form of an increased probability of being preyed upon while

foraging for female needs. The data on Snow Buntings are simply too
limited to address this point.
Male European Sparrowhawks (Accipiter nisus) provide all food
for incubating females and continue to feed brooding females into the
early nestling period. Newton et a1. (1983) suggested that male ability
to hunt and provide food for females may directly influence breeding
success. Poorly provisioned females first rely on stored energy reserves,
then hunt for themselves, resulting in nest desertion.
Nisbet (1973) found that the amount of courtship feeding of females
by male Common Terns (Sterna hirundo) was correlated with total fresh
weight of the subsequent clutch. Fledging success was correlated with
egg size, which probably reflected the quality of male courtship feeding.
Furthermore, a male's level of courtship feeding was correlated with
his subsequent level of nestling feeding, which was, in turn, correlated
with the weight of early nestlings at an age when males provide most
of their food.
4.3.3. Mate Protection and Female Health

A subject that has received little consideration is the possible as-
sociation between PI patterns by the sexes and the advantages of long-
term pair bonding in monogamous species (Freed, 1987). Dring (1982)
appears to be one of the few investigators who has recognized impli-
cations of this association (see also Smith, 1980; Shields, 1984; Regel-
mann and Curio, 1986). Where there is an advantage to long-term pair
bonding, the health of the mate becomes important in influencing par-
enting patterns to favor the maintenance of a long-term pair bond.
If female mortality is high for reasons other than PI, males should
expend high levels of investment, in order to increase the probability
that a mate will survive into the next breeding season. Advantages to
such males will be significant if either (1) the influence of reproductive
costs on female survival in the nonbreeding season, or (2) long-term
bonding, strongly contributes to male lifetime reproductive success.
Even if a male increases his probability of dying as a result of increased
PI, high paternal investment can evolve if reproductive success at early
ages is favored (Cole, 1954; R. Breitwisch, unpublished data).
By this reasoning, there may be many species of monogamous birds
that fulfill these preconditions for high levels of male PI. Unfortunately,
we still know relatively little about the frequency of long-term pair
bonds in monogamous biparental passerines. In my own study of mock-
ingbirds, I have recorded a few pairs remaining together at least 7 or 8
years (R. Breitwisch, unpublished data; P. G. Merritt, unpublished data),

suggesting at least an occasional occurrence of such long-term pair
bonding.
4.4. Further Complications

There are additional complications to assessing PI by the sexes.
Relative PI between mates may change with either brood size or en-
vironmental conditions. Hails and Bryant (1979) found that the increase
in energy expenditure with increasing brood size was greater for male
parents than for females in House Martins (Delich on urbica). Witten-
berger (1982) found that relative nestling feeding rates by the sexes
changed among years in Bobolinks (Dolichonyx oryzivorus). Male Bob-
olinks increased their relative rates with good weather and scarce food
availability.
Recent investigations have demonstrated that there can be sub-
stantial differences among individuals within populations of monog-
amous, biparental birds in both the relative and absolute levels of pa-
rental care (e.g., Burley, 1977; Drent and Daan, 1980; Greig-Smith, 1982;
Breitwisch, 1988). These findings should serve as an admonishment;
in any investigation of PI, marked individuals are a necessity, and
sample sizes must be large enough to take into account large interin-
dividual differences in parental care.
4.5. Case Histories

We have limited data on sex roles in parental care for monogamous,
biparental birds. Obviously, we have extensive data on particular com-
ponents of parental care for many species, but the need for reasonably
complete data for anyone species on all major aspects of PI is stressed.
A few species have been studied with such a broad approach.
4.5.1. Canvasback Duck

Anderson (1984, 1985) studied parental care and pair-bond behav-
ior in Canvasback Ducks. This dimorphic, monogamous diving duck
is characterized by male-biased tertiary sex ratios. Nesting mortality of
females is relatively low, even though females are responsible for in-
cubation and all post-hatching parental care. PI by males occurs prior
to hatching as indirect parental care in (1) dominance at feeding sites
allowing mates to feed undisturbed; and (2) mate protection against
predators, conspecific males attempting forced copulations, and brood-
parasitic Redheads (Aythya americana).
Anderson estimated time and energy budgets and observed pair-

bond reinforcement behavior at different stages of the nesting cycle. He
calculated cumulative reproductive effort for males versus females, in-
cluding mating effort in his calculations. Anderson claimed that cu-
mulative reproductive effort curves showed higher overall expenditure
by females (1984) and that PI by females was greater than male PI (1985).
Furthermore, sex differences in desertion tendencies versus pair-bond
maintenance activities and changes in these during stages of the nesting
cycle fit Trivers's (1972) predictions from PI theory. However, Anderson
did not present any data on cumulative energy expenditure, only "qual-
itative" comparison in figures. It is therefore difficult to assess the
shapes and steepness of the cumulative energy expenditure curves.
Assumptions made by Anderson in his comparison of the sexes
warrant discussion. First, he assumed that energy expenditure is an
appropriate measure of PI; there was no attempt to measure risk-taking
behavior. Yet, male Canvasbacks engage in significant protection of the
female. Is there a risk of injury in establishing dominance at a feeding
area in which a mate can then accumulate nutritional stores for egg
building? Is there risk of predation in being the more vigilant member
of the pair against predators and giving more warning calls in the pres-
ence of predators? Anderson noted the potential importance of these
aspects of male behavior to females but did not otherwise assess them.
Second, Anderson apparently included all behavior during the nesting
cycle as reproductive effort (the methods are not explicit on this point).
The assumption must be that all behavior of parents during the nesting
cycle is relevant to any estimate of reproductive effort. Anderson in-
cluded mating effort in this estimate. Because he was interested in
questions of desertion, this inclusion is warranted, but it tells us little
about the subset of reproductive effort that is parental effort (PI), es-
pecially because male Canvasbacks spend a significant amount of time
courting females other than their mate. Insofar as pertinent aspects of
male PI were not measured, we still lack estimates of PI by the sexes
in Canvasbacks.
Canvasback females renest if their first nest is preyed upon, and
there is a strong tendency to remain with the same male. This choice
by females indicates that preincubation indirect parental care (PI) by
males may be a significant determinant in favoring pair maintenance
between nestings.
4.5.2. American Oystercatcher

Nol (1985) compared sex roles in parental care in the American
Oystercatcher. She constructed detailed time and energy budgets for
males and females, then compared these at different stages in the nest-
ing cycle. Her conclusion was that male and female roles in parental
care are similar. Roles diverged during egg laying, with males engaging
in more conspecific chases (suggesting that male chasing is involved
in preventing cuckoldry). Females incubated more than males, but males
surpassed females in overall chases during the chick stage and in pro-
visioning the chicks. The expenditure of energy during the breeding
season was similar for the sexes. Nol suggests that divergence by the
sexes in parental care is explained by different energetic efficiencies of
males and females (males are smaller) in different tasks. The adult
survival rates of the sexes appear similar, but whether this implies a
tertiary sex ratio of unity is not clear.
Nol explicitly states the assumptions used in estimating cumulative
investment curves for the sexes during the breeding season. First, it
was assumed that cumulative energy expenditure is an appropriate
measure of PI. Second, it was assumed that every aspect of behavior
during the breeding season is related to fledging offspring, thus qualifies
as PI. These assumptions are controversial. The first does not allow for
measuring risk-taking behavior, yet investigators since Trivers have
realized the importance of attempting to assess risk. Second, Nol's de-
cision as to which aspects of behavior to include in PI is an extreme
view. Suppose that a male spent a significant amount of time and energy
attempting to secure extra-pair forced copulations during the breeding
season. While this behavior may well relate to "fledging offspring" (Nol,
1985), it hardly qualifies as PI. Yet, by Nol's measure, it would be
included.
Despite these criticisms, I find it intriguing that the mortality sched-
ules suggest a tertiary sex ratio of unity; there does not appear to be a
scarcity of females, and PI appears to be similar for the sexes. None-
theless, I believe we still need to assess individual components of PI
in Oystercatchers, particularly the defense of offspring against preda-
tors.
4.5.3. Great Tit

Great Tits are small, monomorphic, monogamous passerines. Cer-
tainly one of the best-studied passerines, the Great Tit is known to
display male-biased tertiary sex ratios (Orell and Ojanen, 1979; Curio
and Regelmann, 1982; Regelmann and Curio, 1986). Adult female mor-
tality is higher than male mortality in both the breeding and nonbreed-
ing seasons (E. Curio, personal communication).
Brood defense by Great Tits has been studied intensively by Curio
and his collaborators (e.g., Curio, 1980; Regelmann and Curio, 1986,
and references cited therein). Males surpass females in various aspects
of brood defense, including approaching a predator both more quickly
and more closely, and displaying a shorter delay to the initiation of
calling in defense. Males presumably thereby take greater risks than
females in defense. Males display even greater levels of defense when
the mate is present, suggesting protection of the female and/or display
to the female of physical abilities in parental care as an additional
function of defense (Regelmann and Curio, 1986).
Royama (1966b) conducted an intensive study of nestling feeding
by Great Tits in a different population. He found that males provided
a greater biomass of food than did females to nestlings, despite a lower
feeding rate. Royama's findings of greater load size in food delivery by
males indicates that previous results by Kluyver (1950) and Hinde (1952)
in different populations may need to be reassessed in comparing nest-
ling feeding by males versus females as a component of PI.
Last, Kluyver et a1. (1977) have shown that male Great Tits are
largely responsible for the care of fledglings when females begin in-
cubating second clutches. Thus, males expend significant additional PI
in feeding and protecting offspring during a period early in which
female PI has ended.
4.5.4. Stonechat
Greig-Smith (1980, 1982) studied parental care in Stone chats , a
small, dimorphic, monogamous passerine. Although he did not provide
an estimate of the adult sex ratio, Greig-Smith (1980) noted that mated
females who were killed (disappeared?) during the breeding season
were not replaced, suggesting a male-biased, tertiary sex ratio. Further
evidence of skewing was the presence of unmated, territorial males
through the breeding season (1982).
Greig-Smith (1980) found that levels of nest defense (primarily
consisting of calls) were similar between males and females. However,
of the two types of calls given, one appears to be more effective in
distracting predators from nests toward the caller, and, in this way,
may involve greater risk to the caller. Males gave this call at a higher
rate that females at the time of fledging. This disparity also occurred
while females incubated the successive clutch.
Greig-Smith (1982) also found that males with higher song rates
prior to pair formation subsequently provided a greater proportion of
feedings to nestlings. Overall, males provided more feedings to nest-
lings than did females; I estimate the mean percentage as 59% (Greig-
Smith, 1982; Fig. 6). Together, these findings indicate that male PI is
crucial to nesting success in Stonechats, and females may choose mates
on the basis of male signals predicting future levels of PI by males (see
also Searcy, 1979b, 1982; Searcy and Andersson, 1986).
4.5.5. Northern Mockingbird

Several components of parental care have been studied in the same
population of Northern Mockingbirds. This monomorphic species is
essentially monogamous; approximately 5% of males are bigamous in
a southern Florida population (Breitwisch et a1., 1986c). In this pop-
ulation, the adult sex ratio is male biased. In each of eight successive
breeding seasons (1980-1987), the adult sex ratio was at least 1.25
(Merritt, 1985; Breitwisch et a1., 1986b; R. Breitwisch, unpublished
data). This sex ratio is in territorial adults; i.e., surplus males hold
territories. Although there may also be floater males, further skewing
the sex ratio, there appear not to be floater females (Merritt, 1985).
Similar male-biased adult sex ratios in populations of monogamous
mockingbirds are found in North Carolina (c. A. Logan, personal com-
munication) and New York (J. Utter, personal communication).
Breitwisch et a1. (1986b) measured parental feeding rates to nest-
lings and found that males fed nestlings at rates similar to females.
Moreover, males fed more in the middle third of the nestling period
when young grow most rapidly and their nutritional needs are greatest.
Males predominated in fledgling care. They fed fledglings more
food than females and for a longer period (Zaias and Breitwisch, 1988).
Female mockingbirds fed fledglings until the subsequent nest of the
season was built, occasionally fed at low levels during the 3-4 days of
egg laying, and stopped only when they initiated incubation (Zaias and
Breitwisch, 1988). These observations suggest that energy and/or time
demands on females become critical only when incubation begins.
A mockingbird egg weighs about 10% of a female's body weight
(4.5 g versus -47 g), and a female can begin to lay a new clutch several
days after predation on a previous clutch or brood. A female can lay
at least six clutches of three to four eggs in the 5- to 6-month breeding
season in southern Florida (R. Breitwisch, unpublished data). There
was no seasonal decline in clutch size, nor was there any increase in
time between successive clutches (R. Breitwisch, unpublished data).
These observations suggest that egg production by female mockingbirds
is not energetically expensive.
Males defended eggs, nestlings, and fledglings against predators
more strongly than did females. Differences between the sexes included
greater frequency of attacks on potential predators by males (Breitwisch,

1988; Zaias and Breitwisch, 1988). Pairs in which males strongly at-
tacked human intruders acting as potential predators of young expe-
rienced greater nesting success than pairs in which males did not attack
or attacked weakly (Breitwisch, 1988).
Male and female mockingbirds displayed different compromises
between predator avoidance and nestling feeding (R. Breitwisch, N.
Gottlieb, and J. Zaias, unpublished data). Males approached nests with
food items more slowly, visually scanning the immediate area before
delivery. Females did not engage in this scanning activity, and their
food delivery was more rapid. Males vocalized when predators were
visible near the territory, and females responded by approaching the
nest in food delivery more slowly.
In summary, the information on PI by male and female mocking-
birds supports the hypothesis that males invest more time and energy
and assume greater risks in caring for offspring than do females. Males
(1) peak in their feeding rates when nestlings grow most rapidly, (2)
feed fledglings more than do females; (3) defend eggs, nestlings, and
fledglings more strongly than do females; and (4) are more vigilant than
females when caring for nestlings. Existing theory would thus predict
males to be the limiting sex. Yet males actively fight for territorial space
necessary for attracting a mate (Howard, 1974; Merritt, 1985; Breitwisch
et al., 1986a; Breitwisch and Whitesides, 1987) and in this way compete
for access to females. There is currently no evidence that females com-
pete for mates.
4.6. Conclusions
There are relatively few species of monogamous biparental birds
for which we have extensive data on all major components of PI (vide
supra). The case histories are offered not as strict tests of the predictions
of hypotheses. Rather, these have been provided as evidence for the
plausibility of extensive paternal care in monogamous birds, and, by
inference, the suggestion of high male PI. My primary conclusion is
that there is a lack of evidence to support a general assumption of high
female PI relative to male PI. Males have been observed to take major
roles in feeding nestlings and fledglings and in defending eggs, nest-
lings, and fledglings against predators. These observations should, at
the very least, whet our appetites for more data on the roles of the sexes
in parental care in monogamous biparental birds. My second conclusion
is that we need information on the several primary components of
o
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«0+
11:'
>1
=I--~---
/
x_0
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{-
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- - - -
FIGURE 1. Skewing of the sex ratio
(males-females): (a) resulting from differential
adult mortality of the sexes, and (b) resulting
from differential juvenile mortality of the sexes.
x_
w The horizontal, long, dashed line in each de-
en
<I notes a sex ratio of unity. Three possible tra-
jectories of the sex ratio subsequent to initial
skewing are indicated in (b) by short, dashed
AGE OF A COHORT lines.
PI expended by males and females in the same populations. Only by

assessing all the major aspects of PI, controlling for population differ-
ences, yearly fluctuations in environmental conditions, and brood size
within populations, can we expect to be able to compare PI by males
and females.
5. DISCUSSION
5.1. Testing Predictions of Alternative Hypotheses

The primary question still unanswered is when and how female
birds die. To recapitulate, there are three hypotheses to account for
male-biased tertiary sex ratios in monogamous birds: females may suffer
greater mortality than males (1) as juveniles, (2) as adults from causes
not related to PI, or (3) as adults from PI. The prediction from the first
two hypotheses is relatively high male PI because surviving females
demand this of their mates. Should this be found, one needs to deter-
mine the schedule of skewing in the sex ratio in order to choose between
alternative hypotheses. The primary prediction of the third hypothesis
is relatively high female PI.
,--------~-~~---------------I
NON BREEDING SEASON

MORT ALIT; PREDOMINANT I
BREEDING SEASON ( I
~: . " " ' ' ' \ ' : ' ~n •• _ + I
B-1 B-2 B-3

AGE OF A COHORT
FIGURE 2. Skewing of the adult sex ratio (males-females) resulting from breeding season
versus nonbreeding season mortality. The horizontal. long, dashed line denotes a sex
ratio of unity. B-1 through B-3 are the first three breeding seasons for this cohort.
I have displayed alternative sources and consequences of skewing

the population sex ratio in Figs. land 2. The hypothesis of greater
female PI predicts skewing as displayed in Fig. la. The sex ratio does
not begin to depart significantly from unity until breeding age. Some-
time after breeding begins in a cohort, females die on an earlier schedule
than males due to high female PI. The result is an increasing departure
from unity as the cohort ages. The hypothesis of greater female mortality
in juveniles is displayed as a skewing of the juvenile sex ratio (Fig. lb).
The relative scarcity of females in this cohort entering the breeding
population is to some degree ameliorated with time as males suffer
disproportionate mortality from relatively high PI. Depending on the
severity of departure of the juvenile sex ratio from unity, and perhaps
other factors, the sex ratio of this cohort may change further with age.
This change could follow anyone of many possible trajectories, three
of which are displayed in Fig. lb. In this manner, mortality patterns of
juveniles determine subsequent parenting patterns, or relative levels of
PI, by individuals surviving into adulthood.
Detailed documentation of survivorship in the sexes would allow
testing the predicted patterns of mortality by these two models. The
strongest tests would include information on the causes of death and
their relative importance along with analysis of the reproductive costs
of all major aspects of parental care. Obviously, this is a major under-
taking, and it is not surprising that we do not have this set of information
for any species of bird.
The schedules of mortality for the sexes must be determined with
a high degree of resolution. Simply establishing that skewing of the sex
ratio occurs in adults rather than juveniles would provide enough in-
formation to reject the juvenile mortality hypothesis, but not enough
to reject the second hypothesis of adult deaths due to non-PI causes.
Thus, an increasingly skewed sex ratio in an aging cohort is not in itself
evidence for greater PI by members of the less common sex. Figure 2
diagrams the alternative schedules of mortality in adults that would
lead to a male-biased sex ratio. The alternative mortality pulses are in
the breeding versus nonbreeding seasons and simple step functions
proposed. Obviously, real mortality patterns are more complex. The
logistical difficulty in determining when and how these deaths occur
is simply emphasized.
The operational difficulty in distinguishing between mortality re-
lated to PI and other causes of mortality is considerable but does not
diminish the theoretical importance of this distinction. If higher mor-
tality in one sex is attributable to deaths unrelated to breeding biology,
members of that sex behaviorally can demand high levels of PI by
members of the more common sex (see also Knowlton, 1979, 1982;
Petrie, 1983a). As the former sex becomes even rarer, surviving mem-
bers of that sex can demand increasing levels of PI from members of
the opposite sex. Relatively scarce females in monogamous species may
thereby demand significant paternal care of offspring, under the threat
of desertion. Relatively abundant males do not have this option and
must accede to female demands (Breitwisch et 01., 1986b; Breitwisch,
1988; S. Rohwer and V. Nolan, unpublished data). Males unable to
expend such levels will either remain unmated or be deserted by their
mates in favor of males expending at least the mean level of PI in the
male population (Diamond, 1987). No prediction is made here of which
components of PI should show the greatest male predominance, only
that total male PI should exceed total female PI.
In Northern Mockingbirds, females occasionally desert their mates
following nest predation (R. Breitwisch, unpublished data; see Rowley,
1983). Nesting success is related to the strength of male defense of
offspring (Breitwisch, 1988), and a female would be advantaged if able
to monitor male aggression prior to pair formation. Nevertheless, there
may be additional individual differences in female quality restricting
choice of mates for some females (Burley, 1977; Breitwisch, 1988).
Furthermore, advantages to long-term or lifetime monogamy (Oring,
1982; Rowley, 1983) may counteract desertion.
The two novel hypotheses outlined here are an extension of Emlen

and Gring's (1977) model. Their argument emphasizes the importance
of the "environmental potential for polygamy" as a determinant of a
population's mating system. I have dealt here with monogamous species
of birds in which, presumably, the environmental potential for polyg-
amy is low. The hypotheses extend Emlen and Gring's concept of the
operational sex ratio to predict relative levels of PI by the sexes in
monogamous birds. In species in which PI patterns by the sexes are
known, the prediction is that where male PI is greater than female PI,
the adult sex ratio should depart from unity in the direction of fewer
females (see Murray, 1984). Walsberg (1983a: Table X) provides relative
PI levels by the sexes for eight species of monogamous passerines.
Taking the extremes of this group, I predict that Black-billed Magpies
(Pica pica), with relatively high male PI, display a scarcity of females,
and that Red-eyed Vireos (Vireo olivaceus), with relatively low male
PI, display no such scarcity.
5.2. Why Aren't More Birds Polyandrous?

Given that tertiary sex ratios in monogamous birds frequently are
male biased, why aren't more birds polyandrous? Avian polyandry is
rare (Ridley, 1978; Gring, 1986), yet theoretically, polyandry can ad-
vantage members of both sexes (however, see Erckmann, 1983). De-
pending on egg cost (see Graul et aI., 1977), a female could lay clutches
for two or more males, if each male were able to provide most of the
necessary parental care for his offspring. A female could thereby in-
crease her reproductive success dramatically. The male who, in the
absence of polyandry, would be unmated because of a skewed sex ratio
obviously could benefit from polyandry if his probability of becoming
mated increased (Murray, 1984, 1985b). Gn the other hand, what costs
would be paid in polyandry by a male who in a monogamous system
has reasonable prospects for being mated (Erckmann, 1983)?
Gring (1986) ably reviewed the topic of avian polyandry. He dis-
tinguished between two general types of polyandry: (1) classical, in
which males breed solitarily with a female, yet females divide their
activities among males, and (2) cooperative, in which groups of males
share a single breeding effort with a female. Classical polyandry occurs
most frequently in shorebirds, while cooperative polyandry occurs spo-
radically in more varied taxonomic groups. Gring stated that any ex-
planation for the evolution of classical polyandry must explain why
males provide uniparental care. He turned to a model of mate desertion
and PI in which Maynard Smith (1977) showed that uniparental care
by males and female desertion depended on (1) the (operational) sex

ratio, (2) the increase in female fecundity with desertion, and (3) ben-
efits of uniparental care for offspring, but little additional advantage to
offspring of biparental care. The evolution of cooperative polyandry
depends upon some combination of kin selection and environmental
conditions that favor living in groups.
~ring (1986) concluded that polyandry is rare in birds because
females require substantial resources to reproduce, and thus have lim-
ited ability to monopolize males, as opposed to limited constraints on
males in the evolution of polygyny. Our limited knowledge of PI pat-
terns in monogamous birds suggests that males may invest heavily in
parental care. If so, which requirements of females for breeding prevent
their monopolizing more than one male? Is time, energy, or mineral
storage most critical for breeding females? There is reason to question
an assumption of a large energy cost to breeding for females in mo-
nogamous birds. The time and energy invested in breeding by monog-
amous males may surpass that invested by monogamous females; this
question remains unanswered. Certainly, tertiary sex ratios favor po-
lyandry (Maynard Smith, 1977; Murray, 1984, 1985b), for females have
alternative mating opportunities. Nor is biparental care necessary for
raising offspring in most species (Wittenberger and Tilson, 1980), al-
though reproductive success may be greater with two parents than with
uniparental care.
G. Hausfater and L. W. Oring (unpublished data) have investigated
the evolution of classical polyandry via a model involving computer
simulations. They altered values taken by three variables: (1) a male-
biased tertiary sex ratio, (2) a "single parent disadvantage" of females
relative to males, and (3) a "second mating disadvantage" experienced
by males who desert a first nest after some investment in uniparental
care and are thus disadvantaged in attempts to secure second mating
relative to males who have not yet received a clutch. Of these three
factors, the strength of skew in the sex ratio was the most effective in
leading a monogamous population into polyandry. A sex ratio of 1.5,
for instance, led to fixation of the population in a polyandrous con-
dition, but even slight male bias appreciably increased the probability
that the population would become polyandrous.
The power of a male-biased sex ratio to influence the evolution of
polyandry in this model is noteworthy. Hausfater and Oring point out
that 1.5 is also the approximate sex ratio in a large polyandrous pop-
ulation of Spotted Sandpipers in north central Minnesota. In their treat-
ment, Hausfater and Oring discuss the possibility that sex ratio may,
in fact, be the key element in the evolution of polyandry.
This simulation study should increase the interest of investigators

of mating systems and PI in the reasons for male-biased sex ratios in
monogamous, biparental birds. Tertiary sex ratios in some populations
of these species appear to be well within the range of values favoring
polyandry. Yet, sex ratios have generally been viewed as simply the
result rather than the cause of mating systems and parenting patterns
(however, see Smith et a1., 1982; Murray, 1984, 1985b; G. Hausfater
and L. W. Oring, unpublished data). Perhaps, the advantages of bipar-
ental versus uniparental care in monogamous species are great enough
to disfavor female desertion (see Maynard Smith, 1977; Wittenberger
and Tilson, 1980). And, yet, one wonders how "near" to polyandry
many monogamous populations may be located on their adaptive land-
scapes. Might we expect to observe occasional polyandrous females in
otherwise monogamous populations?
Fulk et a1. (1987) recently provided the first report of a polyandrous
female Northern Mockingbird. This female incubated all clutches, and
provided some parental care for nestlings hatched on territories of two
neighboring males. She had apparently engaged in a polyandrous re-
lationship for at least 2 years. The male-biased sex ratio in this popu-
lation (c. A. Logan, personal communication) may have been instru-
mental in making available an unmated neighboring male. The typical
high level of male PI in Northern Mockingbirds may also have mini-
mized the cost of partial desertion by a female.
It may not be fortuitous that the population in which this case of
polyandry was documented has been under continuous observation for
nearly ten years. Such long-term studies on single populations could
be our most likely source of similar observations. Witness, for instance,
the fascinating mixture of mating relationships in Dunnocks (Prunella
modularis) (Davies and Lundberg, 1984; Davies, 1985; summarized by
Brown, 1987).
5.3. Conclusions and Prospectus

From the survey of available information on the topics of sex ratios,
mortality patterns, and PI in monogamous, biparental birds, the follow-
ing general conclusion are drawn: (1) adult sex ratios are male biased
in many such species; (2) sex ratios become male biased after the ter-
mination of parental care (in some species, this may occur in juveniles;
in others, it appears to occur in adults; it may occur in both juveniles
and adults for some species); (3) in general, we know neither the pri-
mary sources of mortality for male versus female birds after the ter-
mination of parental care nor whether these change with age; (4) dif-
ferential mortality in adults may occur frequently in the nonbreeding

season when mortality is greater for females (we do not know whether
this is delayed payment by females for previous PI), and (5) we possess
data on patterns of PI by males versus females for no more than several
species of monogamous biparental birds. In general, these data are too
scant to permit realistic searching for patterns among species.
Clearly, data are needed to test among the hypotheses discussed
in this paper. For any biparental monogamous bird, we need detailed
information on sex roles in parental care, the causes of death of males
and females, and resulting sex ratios. The problem of disappearing
females is critical enough that investigators should consider working
on populations located on isolated islands on which the closed nature
of these populations allows stronger inference of death. Three different
schedules of significant mortality of females-deaths before breeding
versus nonbreeding-related adult deaths versus breeding-related deaths-
are all plausible. If either or both of the first two predominate, PI theory
must be modified to incorporate mortality patterns and resulting sex
ratios.
ACKNOWLEDGMENTS. Andy Dobson, Ted Fleming, Patty Gowaty, Steve

Green, Peter Merritt, Bert Murray, Lew Dring, Alan Smith, Keith Wad-
dington, and George Whitesides critically reviewed previous versions
of this paper. My thanks are not meant to imply that they agree com-
pletely with my interpretations. I thank the following for discussion of
ideas: Nancy Burley, Brian Charlesworth, Eberhard Curio, Jan Ekman,
Ted Fleming, Patty Gowaty, Steve Green, Richard Johnston, David Li-
gon, Bert Murray, Lew Dring, Bob Ricklefs, Sievert Rohwer, and Bill
Searcy. Bert Murray has previously explored some of the questions
raised here, and I believe his papers deserve more attention than they
have received from students of mating systems and parenting patterns.
lowe special thanks to Robert Trivers for putting forth such provocative
ideas and predictions in his 1972 paper. Linda Hetrick typed the many
drafts of this manuscript. I appreciate the patience displayed by Dennis
Power, the editor of this volume. This work represents contribution
No. 289 in Behavior, Ecology, and Evolution, from the Department of
Biology at the University of Miami.
REFERENCES
Aierstam, T., and Hiigstedt, G., 1984, How important is clutch size dependent adult
mortality? Oikos 43:253-254.
Anderson, M. G., 1984, Parental investment and pair-bond behavior among Canvasback
Ducks (Aythya valisineria, Anatidae), Behav. Ecol. Sociobiol. 15:81-90.
Anderson, M. G., 1985, Variations on monogamy in Canvasbacks (Aythya valisineria),
Ornithol. Monogr. 37:57-67.
Andersson, M., Wiklund, C. G., and Rundgren, H., 1980, Parental defence of offspring:
A model and an example, Anim. Behav. 28:536-542.
Ar, A., and Yom-Toy, Y., 1978, The evolution of parental care in birds, Evolution 32:
655-668.
Armstrong, E. A., 1965, Bird Display and Behaviour. An Introduction to the Study of
Bird Psychology, 2nd rev. ed., Dover, New York.
Askenmo, c., 1979, Reproductive effort and return rate of male Pied Flycatchers, Am.
Nat. 114:748-753.
Beissinger, S. R, 1987, Anisogamy overcome: female strategies in Snail Kites, Am. Nat.
129:486-500.
Bellrose, F. c., Scott, T. G., Hawkins, A. S., and Low, J. 8., 1961, Sex ratios and age ratios
in North American Ducks, Bull. Ill. Nat. Hist. Surv. 27:391-474.
Biedenweg, D. W., 1983, Time and energy budgets ofthe Mockingbird (Mimus polyglottos)
during the breeding season, Auk 100:149-160.
Boag, P. T., and Grant, P. R, 1981, Intense natural selection in a population of Darwin's
Finches (Geospizinae) in the Galapagos, Science 214:82-85.
Boag, P. T., and Grant, P. R, 1984, Darwin's Finches (Geospiza) on Isla Daphne Major,
Galapagos: Breeding and feeding ecology in a climatically variable environment,
Ecol. Monogr. 54:463-489.
Bourliiire, F., 1950, Essquisse ecologique, in: Traite de Zoologie, Tome XV, Oiseaux (P.-
P. Grasse, ed.), Masson et Cie, Paris, pp. 757-791.
Breitwisch, R, 1988, Sex differences in defence of eggs and nestlings by Northern Mock-
ingbirds (Mimus polyglottos), Anim. Behav. 36:62-72.
Breitwisch, R, and Hudak, J., 1989, Sex differences in risk-taking behavior in foraging
flocks of House Sparrows, Auk (In press).
Breitwisch, R, and Whitesides, G. H., 1987, Directionality of singing and non-singing
behaviour of mated and unmated Northern Mockingbirds, Mimus polyglottos, Anim.
Behav. 35:331-339.
Breitwisch, R, Diaz, M., Gottlieb, N., Lee, R, and Zaias, J., 1986a, Defense offall territories
by mated and unmated Northern Mockingbirds in southern Florida, J. Field Ornithol.
57:16-21.
Breitwisch, R, Merritt, P. G., and Whitesides, G. H., 1986b, Parental investment by the
Northern Mockingbird: Male and female roles in feeding nestlings. Auk 103:152-159.
Breitwisch, R, Ritter, R C., and Zaias, J., 1986c, Parental behavior of a bigamous male
Northern Mockingbird, Auk 103:424-427.
Breitwisch, R, Diaz, M., and Lee, R, 1987, Foraging efficiencies and techniques of ju-
venile and adult Northern Mockingbirds (Mimus polyglottos), Behaviour 101:225-235.
Brown, J. 1., 1969, Territorial behavior and population regulation in birds, Wilson Bull.
81:293-329.
Brown, J. 1., 1987, Helping and Communal Breeding in Birds, Princeton University Press,
Princeton, New Jersey.
Bryant, D. M., 1979, Reproductive costs in the House Martin (Delichon urbica), J. Anim.
Ecol. 48:655-675.
Bull, J. J., 1983, Evolution of Sex Determining Mechanisms, Benjamin/Cummings, Menlo
Park, California.
Burley, N., 1977, Parental investment, mate choice, and mate quality, Proc. Natl. Acad.
Sci. USA 74:3476-3479.
Burley, N., 1982, Facultative sex-ratio manipulation, Am. Nat. 120:81-107.
Burley, N., 1986, Sex-ratio manipulation in color-banded populations of Zebra Finches,
Evolution 40:1191-1206.
Charman, K., 1965, Studies on the communal roosting of Starlings (Sturn us vulgaris L.),
Ph.D. thesis, University of Durham, Durham.
Charnov, E. L., 1982, The Theory of Sex Allocation, Princeton University Press, Princeton,
New Jersey.
Clutton-Brock, T. H., 1986, Sex ratio variation in birds, Ibis 128:317-329.
Clutton-Brock, T. H., Guinness, F. E., and Albon, S. D., 1982, Red Deer. Behavior and
Ecology of Two Sexes, University of Chicago Press, Chicago.
Cole, L. C., 1954, The population consequences of life history phenomena, Q. Rev. BioI.
29:103-137.
Coulson, J. C., 1960, A study of the mortality of the Starling based on ringing recoveries,
J. Anim. Ecol. 29:251-271.
Craig, A. J. F. K., and Manson, A. J., 1979, Sex ratios among three Euplectes species in
southern Africa, Ibis 121:224-227.
Curio, E. 1980, An unknown determinant of a sex-specific altruism, Z. Tierpsychol. 53:
139-152.
Curio, E., and Regelmann, K., 1982, Fortpflanzungswert und 'Brutwert' der Kohlmeise
(Parus major), J. Ornithol. 123:237-257.
Curio, E., and Regelmann, K., 1986, Predator harassment implies a real deadly risk: A
reply to Hennessy. Ethology 72:75-78.
Darley, J., 1971, Sex ratio and mortality in the Brown-headed Cowbird, Auk 88:560-566.
Darwin, C., 1871, The Descent of Man and Selection in Relation to Sex, John Murray,
London.
Davies, N. B., 1985, Cooperation and conflict among Dunnocks, Prunella modularis, in
a variable mating system, Anim. Behav. 33:628-648.
Davies, N. B., and Lundberg, A., 1984, Food distribution and a variable mating system
in the Dunnock, Prunella modularis, J. Anim. Ecol. 53:895-912.
De Laet, J., 1985, Dominance and aggression in juvenile Great Tits, Parus major major
L. in relation to dispersal, in: Behavioural Ecology. Ecological Consequences of
Adaptive Behaviour (R. M. Sibly and R. H. Smith, eds.), Blackwell, Oxford, pp.
375-380.
De Steven, D., 1980, Clutch size, breeding success, and parental survival in the Tree
Swallow (Iridoprocne bicolor), Evolution 34:278-291.
Dewsbury, D. A., 1982, Ejaculate cost and male choice, Am. Nat. 119:601-610.
Dhondt, A. A., 1970, The sex ratio of nestling Great Tits, Bird Study 17:282-286.
Dhondt, A. A., 1979, Summer dispersal and survival of juvenile Great Tits in southern
Sweden, Oecologia 42:139-157.
Dhondt, A. A., and Huble, J., 1968, Fledgling-date and sex in relation to dispersal in
young Great Tits, Bird Study 15:127-134.
Diamond, J. M., 1987, A darwinian theory of divorce, Nature (Lond.) 329:765-766.
Dobson, A. P., 1987, A comparison of seasonal and annual mortality for both sexes of
fifteen species of common British birds, Ornis Scand. 18:122-128.
Downhower, J. F., 1978, Darwin's Finches and the evolution of sexual dimorphism in
body size, Nature (Lond.) 263:558-563.
Drent, R., 1973, The natural history of incubation, in: Breeding Biology of Birds (D. S.
Farner, ed.J, National Academy of Sciences, Washington, D. C., pp. 262-311.
Drent, R H., and Daan, S., 1980, The prudent parent: Energetic adjustments in avian
breeding, Ardea 68:225-252.
Dunford, C., 1977, Behavioral limitation of Round-tailed Ground Squirrel density, Ecol-
ogy 58:1254-1268.
Eden, S. F., 1987, Natal philopatry of the Magpie Pica pica, Ibis 129:477-490.
Ekman, J., and Askenmo, C., 1986, Reproductive cost, age-specific survival and a com-
parison of the reproductive strategy in two European Tits (genus Parus), Evolution
40:159-168.
Emlen, S. T., 1976, Lek organization and mating strategy in the Bullfrog, Behav. Ecol.
Sociobiol. 1:283-313.
Emlen, S. T., and Dring, L. W., 1977, Ecology, sexual selection, and the evolution of
mating systems, Science 197:215-223.
Erckmann, W., 1983, The evolution of polyandry in Shorebirds: An evaluation of hy-
potheses, in: Social Behavior of Female Vertebrates (S. K. Wasser, ed.), Academic,
New York, pp. 113-168.
Feare, C., 1984, The Starling, Oxford University Press, Oxford.
Fiala, K. L., 1981a, Reproductive cost and the sex ratio in Red-winged Blackbirds, in:
Natural Selection and Social Behavior: Recent Research and New Theory (R. D.
Alexander and D. W. Tinkle, eds.), Chiron, New York, pp. 198-214.
Fiala, K. L., 1981b, Sex ratio constancy in the Red-winged Blackbird, Evolution 35:
898-910.
Fiala, K. L., and Congdon, J. D., 1983, Energetic consequences of sexual size dimorphism
in nestling Red-winged Blackbirds, Ecology 64:642-647.
Fisher, R A., 1958, The Genetical Theory of Natural Selection, 2nd ed., Dover, New
York.
Fleischer, R c., and Johnston, R F., 1982, Natural selection on body size and proportions
in House Sparrows, Nature (Lond.) 298:747-749.
Fogden, M. P. L., and Fogden, P. M., 1979, The role of fat and protein reserves in the
annual cycle of the Grey-backed Camaroptera in Uganda (Aves: Sylviidae), J. Zool.
189:233-258.
Freed, L. A., 1981, Loss of mass in breeding Wrens: Stress or adaptation?, Ecology 62:
1179-1186.
Freed, L. A., 1987, The long-term pair bond of tropical House Wrens: Advantage or
constraint?, Am. Nat. 130:507-525.
Fry, C. H., 1972, The social organisation of Bee-eaters (Meropidae) and co-operative
breeding in hot-climate birds, Ibis 114:1-14.
Fulk, K. R, Logan, C. A., and Hyatt, L. E., 1987, Polyandry in a female Northern Mock-
ingbird, Wilson Bull. 99:286-288.
Gauthreaux, S. A., Jr., 1978, The ecological significance of behavioral dominance, Persp.
Ethology 3:17-54.
Gauthreaux, S. A., Jr., 1982, The ecology and evolution of avian migration systems, in:
Avian Biology, Vol. 6 (D. S. Farner, J. R. King, and K. C. Parkes, eds.), Academic,
New York, pp. 93-168.
Gladstone, D. E., 1979, Promiscuity in monogamous colonial birds, Am. Nat. 114:545-557.
Glucksman, A., 1974, Sexual dimorphism in mammals, Biol. Rev. 49:423-475.
Gowaty, P. A., and Lennartz, M. R, 1985, Sex ratios of nestling and fledgling Red-
cockaded Woodpeckers (Picoides borealis) favor males, Am. Nat. 126:347-353.
Graul, W., Derrickson, S., and Mock, D., 1977, The evolution of avian polyandry, Am.
Nat. 111:812-816.
Greenberg, R, 1980, Demographic aspects of long-distance migration, in: Migrant Birds
in the Neotropics: Ecology, Behavior, Distribution, and Conservation (A. Keast and
E. S. Morton, eds.), Smithsonian Institution Press, Washington, D. C., pp. 493-504.
Greenwood, P. J., 1980, Mating systems, philo patry and dispersal in birds and mammals,
Anim. Behav. 28:1140-1162.
Greenwood, P. J., 1983, Mating systems and the evolutionary consequences of dispersal,
in: The Ecology of Animal Movement (I. R. Swingland and P. J. Greenwood, eds.),
Oxford University Press, Oxford, pp. 116-131.
Greenwood, P. J., and Harvey, P. H., 1976, Differential mortality and dispersal of male
Blackbirds, Ring. Migr. 1:75-77.
Greenwood, P. J., and Harvey, P. H., 1982, The natal and breeding dispersal of birds,
Annu. Rev. Ecol. Syst. 13:1-21.
Greenwood, P. J., Harvey, P. H., and Perrins, C. M., 1979, The role of dispersal in the
Great Tit (Parus major): The causes, consequences and heritability of natal dispersal,
J. Anim. Ecol. 48:123-142.
Greig-Smith, P. W., 1980, Parental investment in nest defence by Stone chats (Saxicola
torquata), Anim. Behav. 28:604-619.
Greig-Smith, P. W., 1982, Song-rates and parental care by individual male Stonechats
(Saxicola torquata), Anim. Behav. 30:245-252.
Hails, C. J., and Bryant, D. M., 1979, Reproductive energetics of a free-living bird, J. Anim.
Ecol. 48:471-482.
Hamilton, W. D., and May, R. M., 1977, Dispersal in stable habitats, Nature (Land.) 269:
578-581.
Harmsen, R., and Cooke, F., 1983, Binomial sex-ratio distribution in the Lesser Snow
Goose: A theoretical enigma, Am. Nat. 121:1-8.
Hausfater, G., and Oring, L. W., Single parent disadvantage, sex ratio, and the evolution
of polyandry in Shorebirds: A computer mode!, unpublished manuscript.
Hensley, M. M., and Cope, J. B., 1951, Further data on removal and repopulation of the
breeding birds in a spruce-fir community, Auk 68:483-493.
Hinde, R. A., 1952, The behaviour of the Great Tit (Parus major) and some other related
species, Behaviour, 2:1-201.
Hiigstedt, G., 1981, Should there be a positive or negative correlation between survival
of adults in a bird population and their clutch size?, Am. Nat. 118:568-571.
Howard, R. D., 1974, The influence of sexual selection and interspecific competition on
Mockingbird song (Mimus polyglottos), Evolution 28:428-439.
Howe, H. F., 1977a, Sex-ratio adjustment in the Common Grackle, Science 198:744-746.
Howe, H. F., 1977b, Egg size, hatching asynchrony, sex, and brood reduction in the
Common Grackle, Ecology 57:1195-1207.
Howe, H. F., 1979, Evolutionary aspects of parental care in the Common Grackle, Quis-
cal us quiscula L., Evolution 33:41-51.
Hughes, B. 0., and Wood-Gush, D. G. M., 1971, A specific appetite for calcium in Domestic
Chickens, Anim. Behav. 19:490-499.
Jeh!, J. R., and Murray, B. G., 1986, The evolution of normal and reverse sexual size
dimorphism in Shorebirds and other birds, Curr. Ornithol. 3:1-76.
Jenkins, D., Watson, A., and Miller, G. R., 1967, Population fluctuations in the Red Grouse
(Lagopus lagopus scoticus), J. Anim. Ecol. 36:97-122.
Johnson, D. H., Krapu, G. L., Reinecke, K. J., and Jorde, D. G., 1985, An evaluation of
condition indices for birds, J. Wildl. Mgmt. 49:569-575.
Johnson, N. K., 1973, Spring migration of the Western Flycatcher with notes on seasonal
changes in sex and age ratios, Bird-Banding 44:205-220.
SEX RA nos AND PARENTAL INVESTMENT 45
Johnston, R. F., and Fleischer, R. C, 1981, Overwinter mortality and sexual size di-
morphism in the House Sparrow, Auk 98:503-511.
Jones, P. J., and Ward, P., 1976, The level of reserve protein as the proximate factor
controlling the timing of breeding and clutch size in the Red-billed Quelea Quelea
quelea, Ibis 118:547-574.
Kemp, A. c., 1978, A review of the hornbills: Biology and radiation, Living Bird 17:
105-136.
Kendeigh, S. c., 1952, Parental care and its evolution in birds, Ill. BioI. Manogr. 22:
1-356.
Ketterson, E. D., and Nolan, V., Jr., 1976, Geographic variation and its climatic correlates
in the sex ratio of Eastern-wintering Dark-eyed Juncos (Junco hyemalis hyemalis),
Ecology 57:679-693.
Ketterson, E. D., and Nolan, V., Jr., 1982, The role of migration and winter mortality in
the life-history of a temperate-zone migrant, the Dark-eyed Junco, as determined
from demographic analyses of winter populations, Auk 99:243-259.
Ketterson, E. D., and Nolan, V., Jr., 1983, The evolution of differential bird migration,
Curro Ornithol. 1:357-402.
King, J. R., 1973, Energetics of reproduction in birds, in: Breeding Biology of Birds (D.
S. Farner, ed.), pp. 78-107, National Academy of Sciences, Washington, D. C.
King, J. R, 1974, Seasonal allocation of time and energy resources in birds, in: Avian
Energetics (R. A. Paynter, ed.), Publication of the Nuttall Ornithological Club No.
15, Cambridge, MA, pp. 4-70.
King, J. R., Farner, D. S., and Mewaldt, 1. R., 1965, Seasonal sex and age ratios in
populations of the White-crowned Sparrows of the race gambelii, Condor 67:489-504.
Kluyver, H. N., 1950, Daily routines of the Great Tit Porus m. major 1., Ardea 38:99-135.
Kluyver, H. N., van Balen, J. H., and Cave, A. J., 1977, The occurrence of time-saving
mechanisms in the breeding biology of the Great Tit, Porus major, in: Evolutionary
Ecology (B. Stonehouse and C. Perrins, eds.), Macmillan, London, pp. 153-169.
Knapton, R. W., 1984, Parental investment: The problem of currency, Can. ]. Zoo I. 62:
2673-2674.
Knowlton, N., 1979, Reproductive synchrony, parental investment, and the evolutionary
dynamics of sexual selection, Anim. Behav. 27:1022-1033.
Knowlton, N., 1982, Parental care and sex role reversal, in: Current Problems ill Socio-
biology (King's College Sociobiology Group, ed.), Cambridge University Press, Cam-
bridge, pp. 203-222.
Koenig, W. D., and Mumme, R. 1., 1987, Population Ecology of the Cooperatively Breed-
ing Acorn Woodpecker, Princeton University Press, Princeton, New Jersey.
Krebs, J. R., 1970, The efficiency of courtship feeding in the Blue Tit Porus caeruleus,
Ibis 112:108-110.
Lack, D., 1954, The Natural Regulation of Animal Numbers, Oxford University Press,
Oxford.
Lack, D., 1966, Population Studies of Birds, Oxford University Press, London.
Lack, D., 19680, Ecological Adaptations for Breeding in Birds, Methuen, London.
Lack, D., 1968b, Bird migration and natural selection, Oikos 19:1-9.
Lamprecht, J., 1987, Female reproductive strategies in Bar-headed Geese (Anser indicus):
Why are geese monogamous'!, Behav. Ecol. Sociobial. 21:297-305.
Landauer, W., 1967, The hatchability of Chicken eggs as influenced by environment and
heredity, Storrs Agr. Exp. Sla. Univ. Conn. Monogr. 1:1-315.
Lessels, C. M., 1986, Brood size in Canada Geese: A manipulation experiment, J. Anim.
Ecol. 55:669-689.
Liberg, 0., and von Schantz, T., 1985, Sex-biased philopatry and dispersal in birds and
mammals: The Oedipus hypothesis, Am. Nat. 126:129-135.
Lidicker, W. Z., Jr., 1975, The role of dispersal in the demography of small mammals,
in: Small Mammals: Their Productivity and Population Dynamics (F. B. Golley, K.
Petrusewicz, and L. Ryszkowski, eds.), Cambridge University Press, Cambridge, pp.
103-128.
Lifjeld, J. T., and Slagsvold, T., 1986, The function of courtship feeding during incubation
in the Pied Flycatcher Ficedula hypoleuca, Anim. Behav. 34:1441-1453.
Ligon, J. D., 1978, Reproductive interdependence of Pifton Jays and Pifton pines, Ecol.
Monogr.48:111-126.
Loman, J., 1980, Brood size optimization and adaptation among Hooded Crows (Corvus
corone), Ibis 122:494-500.
Low, B. S., 1978, Environmental uncertainty and the parental strategies of marsupials
and placentals, Am. Nat. 112:197-213.
Lyon, B. E., and Montgomerie, R. D., 1985, Incubation feeding in Snow Buntings: Female
manipulation or indirect male parental care?, Behav. Ecol. Sociobiol. 17:279-284.
Martin, T. E., 1987, Food as a limit on breeding birds: A life-history perspective, Annu.
Rev. Ecol. Syst. 18:453-487.
Maxson, S. J., and Oring, L. W., 1980, Breeding season time and energy budgets of the
polyandrous Spotted Sandpiper, Behaviour 74:200-263.
Maynard Smith, J., 1977, Parental investment: A prospective analysis, Anim. Behav. 25:
1-9.
Mayr, E., 1939, The sex ratio in wild birds, Am. Nat. 73:156-179.
McGillivray, W. B., 1983, Intraseasonal reproductive costs for the House Sparrow (Passer
domesticus), Auk 100:25-32.
McKinney, F., Cheng, K. M., and Bruggers, D. J., 1984, Sperm competition in apparently
monogamous birds, in: Sperm Competition and the Evolution of Animal Mating
Systems (R. L. Smith, ed.), Academic, New York, pp. 523-545.
McMillen, M. M., 1979, Differential mortality by sex in fetal and neonatal deaths, Science
204:89-91.
Mead, P. S., Morton, M. L., and Fish, B. E., 1987, Sexual dimorphism in egg size and
implications regarding facultative manipulation of sex in Mountain White-crowned
Sparrows, Condor 89:798-803.
Merritt, P. G., 1985, Song function and the evolution of song repertoires in the Northern
Mockingbird, Mimus polyglottos, Doctoral dissertation, University of Miami, Coral
Gables, Florida.
Mock, D. W., 1985, An introduction to the neglected mating system, Ornithol. Monogr.
37:1-10.
Mueller, W. J., 1976, Egg shell and skeletal metabolism, in: Avian Physiology, 3rd ed.
(P. D. Sturkie, ed.), Springer-Verlag, N. Y., pp. 320-326.
Mueller, H. C., and Meyer, K., 1985, The evolution of reversed sexual dimorphism in
size: A comparative analysis of the Falconiformes of the western Palearctic, Curro
Ornithol. 2:65-101.
Murphy, E. c., and Haukioja, E., 1986, Clutch size in nidicolous birds, Curro Ornithol.
4:141-180.
Murphy, M. T., 1986, Body size and condition, timing of breeding, and aspects of egg
production in Eastern Kingbirds, Auk 103:465-476.
Murray, B. G., 1979, Population Dynamics: Alternative Models, Academic, New York.
Murray, B. G., 1984, A demographic theory on the evolution of mating systems as ex-
emplified by birds, Evol. BioI. 18:71-140.
Murray, B. G., 19850, Evolution of clutch size in tropical species of birds, Ornithol.
Monogr.36:505-519.
Murray, B. G., 1985b, The influence of demography on the evolution of monogamy,
Myers, J. H., 1978, Sex ratio adjustment under food stress: Maximization of quality or
numbers of offspring?, Am. Nat. 112:381-388.
Newton, 1., 1973, Finches, Taplinger, New York.
Newton, 1., 1978, Feeding and development of Sparrowhawk Accipiter nisus nestlings,
J. Zool. 184:465-487.
Newton, 1., and Marquiss, M., 1979, Sex ratio among nestlings of the European Sparrow-
hawk, Am. Nat. 113:309-315.
Newton, 1., Marquiss, M., and Village, A., 1983, Weights, breeding, and survival in
European Sparrow hawks, Auk 100:344-354.
Nice, M. N., 1937, Studies in the life history of the Song Sparrow. I. A population study
of the Song Sparrow, Trans. Linn. Soc, NY 4:1-247.
Nisbet, I. C. T., 1973, Courtship-feeding, egg-size and breeding success in Common Terns,
Nature (Lond.) 241:141-142.
Nol, E., 1985, Sex roles in the American Oystercatcher, Behaviour 95:232-260.
Nolan, V., Jr., 1978, The Ecology and Behavior of the Prairie Warbler Dendroica discolor,
Norberg, R. A., 1981, Temporary weight decrease in breeding birds may result in more
fledged young, Am. Nat. 118:838-850.
Norris, R. A., 1958, Comparative biosystematics and life history of the Nuthatches Sitta
pygmaea and Sitta pusilla, Univ. Calif. Publ. Zool. 56:119-300.
Nur, N., 1984, The consequences of brood size for breeding Blue Tits. I. Adult survival,
weight change and the cost of reproduction, ]. Anim. Ecol. 53:479-486.
Orell, M., and Ojanen, M., 1979, Mortality rates of the Great Tit Porus major in a northern
population, Ardea 67:130-133.
Oring, L. W., 1982, Avian mating systems, in: Avian Biology, Vol. 6 (D. S. Farner, J. R.
King, and K. C. Parkes, eds.), pp. 1-92, Academic, New York.
Oring, L. W., 1986, Avian polyandry, Curr. Ornithol. 3:309-351.
Perrins, C. M., 1970, The timing of birds' breeding seasons, Ibis 112:242-255.
Perrins, C. M., 1979, British Tits, Collins, London.
Petrie, M., 19830, Mate choice in role-reversed species, in: Mate Choice (P. Bateson, ed.),
Cambridge University Press, Cambridge, pp. 167-179.
Petrie, M. 1983b, Female Moorhens compete for small fat males, Science 220:413-415.
Pond, C. M., 1977, The significance of lactation in the evolution of mammals, Evolution
31:177-199.
Potts, G. R., 1969, The influence of eruptive movements, age, population size and other
factors on the survival of the Shag (Phalacrocorax aristotelis L.), ]. Anim. Ecol. 38:
53-102.
Price, M. P., 1935, Notes on population problems and territorial habits of Chiffchaffs and
Willow-warblers, Brit. Birds 29:158-166.
Price, T. D., 1984, The evolution of sexual size dimorphism in Darwin's Finches, Am.
Nat. 123:500-518.
Price, T. D., Grant, P. R., Gibbs, H. 1., and Boag, P. T., 1984, Recurrent patterns of natural
selection in a population of Darwin's Finches, Nature (Lond.) 309:787-789.
Regelmann, K., and Curio, E., 1986, Why do Great Tits (Parus major) males defend their
brood more than females do?, Anim. Behav. 34:1206-1214.
Reid, W. V., 1987, The cost of reproduction in the Glaucous-winged Gull, Oecologia 74:
458-467.
Reyer, H.-V., 1980, Flexible helper structure as an ecological adaptation in the Pied
Kingfisher (Ceryle rudis rudis 1.), Behav. Ecol. Sociobiol. 6:219-227.
Reynolds, C. M., 1972, Mute Swan weights in relation to breeding, Wildfowl 23:111-118.
Reznick, D., 1985, Costs of reproduction: An evaluation of the empirical evidence, Oikos
44:257-267.
Richter, W., 1983, Balanced sex ratios in dimorphic altricial birds: The contribution of
sex-specific growth dynamics, Am. Nat. 121:158-171.
Ricklefs, R. E., 1974, Energetics of reproduction in birds, in: Avian Energetics (R. A.
Paynter, ed.), Publication of the Nuttall Ornithological Club No. 15, Cambridge, MA,
pp. 152-297.
Ricklefs, R. E., 1977, On the evolution of reproductive strategies in birds: Reproductive
effort, Am. Nat. 111:453-478.
Ricklefs, R. E., and Hussell, D. J. T., 1984, Changes in adult mass associated with the
nesting cycle in the European Starling, Ornis Scand. 15:155-161.
Ridley, M., 1978, Paternal care, Anim. Behav. 26:904-932.
Rockwell, R. F., Findlay, C. S., and Cooke, F., 1987, Is there an optimal clutch size in
Snow Geese?, Am. Nat. 130:839-863.
Rohwer, S., 1986, Selection for adoption versus infanticide by replacement "mates" in
birds, Curro Ornithol. 3:353-395.
Rohwer, S., and Nolan, V., Jr., 19, Within-season breeding dispersal in Prairie Warblers
and other passerines, unpublished manuscript.
R0skaft, E., 1983, Sex-role partitioning and parental care by the Rook Corvus frugilegus,
Ornis Scand. 14:180-187.
R0skaft, E., 1985, The effect of enlarged brood size on the future reproductive potential
of the Rook, ]. Anim. Ecol. 54:255-260.
R0skaft, E., and Slagsvold, T., 1985, Differential mortality of male and female offspring
in experimentally manipulated broods of the rook, ]. Anim. Ecol. 54:261-266.
Rowley, I., 1965, The life history of the Superb Blue Wren, Malurus cyaneus, Emu 64:
251-297.
Rowley, 1., 1981, The communal way of life in the Splendid Wren, Malurus splendens,
Z. Tierpsychol. 55:228-267.
Rowley, 1., 1983, Re-mating in birds, in: Mate Choice (P. Bateson, ed.), Cambridge Uni-
versity Press, Cambridge, pp. 331-360.
Royama, T., 1966a, A re-interpretation of courtship feeding, Bird Study 13:116-129.
Royama, T., 1966b, Factors governing feeding rate, food requirement and brood size of
nestling Great Tits Parus major, Ibis 108:313-347.
Samson, F. B., 1976, Territory, breeding density, and fall departure in Cassin's Finch,
Auk 93:477-497.
Sasvari, 1., 1986, Reproductive effort of widowed birds, J. Anim. Ecol. 55:553-564.
Schluter, D., and Smith, J. N. M., 1986, Natural selection on beak and body size in the
Song Sparrow, Evolution 40:221-231.
Searcy, W. A., 1979a, Sexual selection and body size in male Red-winged Blackbirds,
Evolution 33:649-661.
Searcy, W, A., 1979b, Female choice of mates: A general model for birds and its appli-
cation to Red-winged Blackbirds (Age1aius phoeniceus), Am. Nat. 114:77-100.
Searcy, W. A., 1982, The evolutionary effects of mate selection, Annu. Rev. Ecol. Syst.
13:57-85.
Searcy, W. A., and Andersson, M., 1986, Sexual selection and the evolution of song.
Annu. Rev. Ecol. Syst. 17:507-533 ..
Searcy, W. A., and Yasukawa, K., 1981, Sexual size dimorphism and survival of male
and female Blackbirds (Icteridae), Auk 98:457-465.
Selander, R. K., 1966, Sexual dimorphism and differential niche utilization in birds,
Condor 68:113-151.
Selander, R. K., 1972, Sexual selection and dimorphism in birds, in: Sexual Selection
and the Descent of Man, 1871-1971 (B. Campbell, ed.), Aldine, Chicago, pp. 180-230.
Shields, W. M., 1982, Phi10patry, Inbreeding, and the Evolution of Sex, State University
of New York Press, Albany.
Shields, W. M., 1984, Barn Swallow mobbing: Self-defence, collateral kin defence, group
defence, or parental care?, Anim. Behav. 32:132-148.
Shreeve, D. F., 1980, Differential mortality in the sexes of the Aleutian Gray-crowned
Rosy Finch, Am. MidI. Nat. 104:193-197.
Silver, R., Andrews, H., and Ball, G. F., 1985, Parental care in an ecological perspective:
A quantitative analysis of avian subfamilies, Am. Zool. 25:823-840.
Simkiss, K., 1975, Calcium and avian reproduction, in: Avian Physiology (M. Peaker,
ed.), Symposium of the Zoology Society of London, No. 35, London, England, pp.
307-337.
Skutch, A. F., 1935, Helpers at the nest, Auk 52:257-273.
Skutch, A. F., 1976, Parent Birds and Their Young, University of Texas Press, Austill.
Slagsvold, T., R0skaft, E., and Engen, S., 1986, Sex ratio, differential cost of rearing young,
and differential mortality between the sexes during the period of parental care:
Fisher's theory applied to birds, Ornis Scand. 17:117-125.
Smith, J. N. M., 1978, Division of labour by Song Sparrows feeding fledged young, Can.
]. Zool. 56:187-191.
Smith, J. N. M., 1981, Does high fecundity reduce survival in Song Sparrows? Evolution
35:1142-1148.
Smith, J. N. M., Yom-Tov, Y., and Moses,R.. 1982, Polygyny, male parental care, and sex
ratio in Song Sparrows: An experimental study, Auk 99:555-564.
Smith, S. M., 1978, The underworld in a territorial Sparrow: Adaptive strategy for floaters,
Am. Nat. 112:571-582.
Smith, S. M., 1980, Henpecked males: The general pattern in monogamy?, J. Field Or-
nithol. 51:55-64.
Stewart, R. E., and Aldrich, J. W., 1951. Removal and repopulation of breeding birds in
a spruce-fir community, Auk 68:471-482.
Stoddard, H. L., 1931, The Bob-white Quail. Its Habits, Preservation, and Increase, Scrib-
ner's Sons, New York.
Sturkie, P. D. (ed.), 1976, Avian Physiology, 3rd ed., Springer-Verlag, New York.
Thompson, C. F., and Nolan. V., 1973. Population biology of the Yellow-breasted Chat
(lcteria virens L.) in southern Indiana, Ecol. Monogr. 43:145-171.
Trivers, R. L., 1972, Parental investment and sexual selection, in: Sexual Selection and
the Descent of Man, 1871-1971 (B. Campbell, ed.), Aldine, Chicago, pp. 136-179.
Tuomi, J., Hakala, T .. and Haukioja, E., 1983. Alternative concepts of reproductive effort,
costs of reproduction, and selection in life-history evolution, Am. Zool 23:25-34.
Velie, W., 1987, Sex differences in sensory functions, Persp. BioI. Med. 30:490-522.
Verner, J., and Willson, M. F., 1969, Mating systems, sexual dimorphism, and the role
of male North American passerine birds in the nesting cycle, Ornithol. Monogr. 9:
1-76.
von Treuenfels, H., 1937; Beitrag zur Brutbiologie des Waldlaubsangers (Phylloscopus
sibilatrix), J. Orn. 85:605-623.
Walsberg, G. E., 1983a, Avian ecological energetics, in: Avian Biology, Vol. 7 (D. S.
Farner, J. R. King, and K. C. Parkes, eds.), Academic, New York, pp. 161-220.
Walsberg, G. E., 1983b, Ecological energetics: What are the questions? in: Perspectives
in Ornithology (A. H. Brush and G. A. Clark, Jr., eds.), Cambridge University Press,
Cambridge, pp. 135-158.
Ward, P., 1965a, Feeding ecology of the Black-faced Dioch Quelea quelea in Nigeria, Ibis
107:173-214.
Ward, P., 1965b, The breeding biology of the Black-faced Dioch Quelea quelea, in Nigeria,
Ibis 107:326-349.
Ward, P., 1965c, Seasonal changes in the sex ratio of Quelea quelea (Ploceidae), Ibis 107:
397-399.
Welty, J. C., 1975, The Life of Birds, 2nd ed., WB Saunders, Philadelphia.
Wiley, R. H., and Rabenold, K. N., 1984, The evolution of cooperative breeding by delayed
reciprocity and queuing for favorable social positions, Evolution 38:609-621.
Williams, G. C., 1979, The question of adaptive sex ratio in outcrossed vertebrates, Proc.R.
Soc. Lond. B 205:567-580.
Winkler, D. W., and Walters, J. R., 1983, The determination of clutch size in precocial
birds, Curro Ornithol. 1:33-68.
Wiseman, A. J., 1975, Changes in body weight of American Goldfinches, Wilson Bull.
87:390-411.
Wittenberger, J. F., 1981, Animal Social Behavior, Duxbury, Boston.
Wittenberger, J. F., 1982, Factors affecting how male and female Bobolinks apportion
parental investments, Condor 84:22-39.
Wittenberger, J. F., and Tilson, R. L., 1980, The evolution of monogamy: Hypotheses and
predictions, Annu. Rev. Ecol. Syst. 11:197-232.
Woolfenden, G. E., and Fitzpatrick, J. W., 1984, The Florida Scrub Jay: Demography of
a Cooperative-breeding Bird, Princeton University Press, Princeton, New Jersey.
Wunderle, J. M., 1984, Mate switching and a seasonal increase in polygyny in the Ban-
anaquit, Behaviour 88:123-144.
Yom-Tov, Y., and Ollason, J. G., 1976, Sexual dimorphism and sex ratios in wild birds,
Oikos 27:81-85.
Zaias, J., and Breitwisch, R., 1988, Intra-pair cooperation, fledgling care, and renesting
by Northern Mockingbirds (Mimus polyglottos), Ethology (in press).
CHAPTER 2
THE EVOLUTION OF
CONSPICUOUS AND DISTINCTIVE
COLORATION FOR
COMMUNICATION IN BIRDS
GREGORY S. BUTCHER and SIEVERT ROHWER
1. INTRODUCTION
Our goal is to elucidate the selective pressures that account for the
origin and maintenance of conspicuous and distinctive coloration
(hereafter referred to collectively as colorfulness) in birds. Our ideas
are relevant to the study of other animals as well. We propose an "ad-
aptationist program" (Gould and Lewontin, 1979) that features the use
of the comparative method (Hailman, 1976; Ridley, 1983; Clutton-Brock
and Harvey, 1984), color manipulations, and tests of a priori predic-
tions. Our major effort is to compare and contrast the major hypotheses
that have been proposed to account for colorfulness in birds. Progress
in understanding bird coloration will come more quickly when re-
searchers evaluate more than one hypothesis at a time. The availability
of multiple hypotheses serves two major purposes. First, it frees the
researcher from psychological dependence on the hypotheses being
tested (Loehle, 1987). Second, with careful planning, it permits strong
inference testing (Platt, 1964) among the most relevant hypotheses.
GREGORY S. BUTCHER and SIEVERT ROHWER • Department of Zoology and Burke

Museum, University of Washington, Seattle, Washington 98195. Present address for
G. S. B.: Cornell Laboratory of Ornithology, Ithaca, New York 14850.
51
52 GREGORY S. BUTCHER and SIEVERT ROHWER
First, we discuss the goals of the review and introduce the com-
parative method and color manipulations as potentially powerful tools
for determining the benefits of conspicuous coloration. Next we define
our major color terms (conspicuous, distinctive, and cryptic) and pro-
vide a short historical overview of coloration theories. In the next three
sections, we discuss five important intraspecific patterns of bird color-
ation that have been well documented and that are exactly the kinds
of patterns for which we hope to provide functional explanations. Four
of the patterns suggest general functional explanations; the fifth pattern
(color dimorphism/polymorphism unrelated to sex or age) seemingly
cannot be explained by a single functional hypothesis. The second half
of this review (1) presents updated versions of a number of color hy-
potheses; (2) discusses the type of evidence required to (a) distinguish
similar hypotheses, (b) provide strong support for a given hypothesis,
or (c) reject a given hypothesis; and (3) presents the evidence currently
available concerning the hypothesis. Because this area of study is rel-
atively undeveloped, there are few adequate tests of hypotheses; there-
fore, we do not dwell on the weaknesses of those that are available.
Although biologists have speculated about the causes of colorful-
ness for many years (see our historical overview below), this area of
study is relatively undeveloped. For instance, hypothesis testing has
been rare and lags dramatically behind hypothesis generation. Most
color hypotheses, as they have been presented to date, have been in-
troduced as plausible explanations, supported by only a few well-cho-
sen examples, not systematic tests of predictions. Rarely has more than
one hypothesis been considered at a time, and rarely have broad in-
terspecific tests been undertaken. We hope that by summarizing the
numerous hypotheses available for testing we can help to move the
field of animal coloration from the era of hypothesis generation to that
of hypothesis testing.
The major tool for ferreting out general causes of the origin of
colorfulness should be the comparative method (elutton-Brock and
Harvey, 1984, and references cited therein). From each hypothesis con-
cerning colorfulness, we can predict a correlation between colorfulness
and one or more ecological or behavioral characteristics of populations.
If the predictions are confirmed in a wide range of taxa, that charac-
teristic may be affirmed as an important cause of colorfulness. The
comparative method provides a useful check on adaptationist zeal by
revealing phylogenetic correlations of traits that indicate that a trait
may be nonadaptive. Unfortunately, few studies of bird coloration have
used the comparative method. One of the major reasons for the lack of
use of the comparative method is that avian phylogenies are currently
CONSPICUOUS COLORATION 53
in much dispute (Cracraft, 1981; Olson, 1982; Sibley and Ahlquist,

1983). Studies of individual species are useful for determining what
the current functions of color might be and for predicting cross-tax-
onomic patterns, but these studies alone cannot help us separate orig-
inal functions from secondary uses of coloration.
A major limitation of the comparative method is that it cannot
prove a functional relationship. Also, because it requires data from a
wide variety of species, the quality of data is not always as high as
might be desired. Thus, broad comparative studies must be supple-
mented by strong intraspecific tests of function. Color manipulations
are an important tool for these intraspecific tests. Each of the color
hypotheses provides a functional explanation for colorfulness from which
the effects of color manipulations can be predicted; if the manipulation
produces the predicted change, it provides strong evidence that the
coloration has the proposed function in that species. Color manipula-
tions might include making an individual look more similar to a syn-
topic congener, making an individual of one age or sex class look as
though it were a member of another class, increasing or decreasing the
conspicuousness of an individual, or obscuring a particular patch of
color.
One limitation of the approach we have taken is that we consider
each hypothesis separately or in pairs in the sections that follow and
make predictions assuming that each hypothesized benefit alone ac-
counted for conspicuousness. It is far more likely that more than one
of the proposed benefits combine to promote the conspicuousness of
animals, and it may be that consideration of each benefit separately
causes us to overlook patterns that reveal important combinations of
causes (Hilborn and Stearns, 1982). On the other hand, there are far
too many hypotheses to consider all possible interactions. Thus, the
first step is to delineate predictions clearly for single hypotheses. If we
are lucky, important causes will create patterns that reveal themselves
despite the interactions of other causes. When an investigator is study-
ing a particular system, many of the hypotheses we consider can be
rejected on a priori grounds, reducing the number of possible benefits
and making the consideration of interactions among possible benefits
more feasible.
1.1. Classifying Coloration: Conspicuous, Distinctive, or

Cryptic
We define signals as sensory cues (e.g., color, vocal, pheromonal)
that have been modified by natural selection to increase the effective-
ness with which they transmit information. This information must mod-
ify the behavior of other organisms such that the signaler benefits, on
average, from the signal. In addition, the receiver must, on average,
benefit from responding to cues that resemble the signal. This definition
has two major implications. First, signals need not be mutually bene-
ficial to senders and receivers. Deceptive signals that induce behavior
that is harmful to the responder are possible and are included in the
definition of a signal. Signals can have high costs to senders as well,
provided they have compensating benefits. Second, signals are different
from signs, which also transmit information to other organisms. By
definition signs have not been modified by natural selection for infor-
mation transfer, and the information they convey may be detrimental
to the individual that generates them. For example, the noise made by
a mouse rustling in the leaves may attract a predator, but mice have
certainly not been designed by natural selection to make such noise.
If an animal's coloration is to function as a signal, it must be either
conspicuous or distinctive (Burtt, 1986). We define distinctive as "un-
usual, easy to distinguish, easy to remember." Any spectrally bright
color or any bold pattern that is rare in the environment should be
distinctive. We define conspicuous as "easy to see at a distance." Large
patches of bright spectral colors, white, or black should all be con-
spicuous, if they contrast with the background against which the co-
loration is viewed. Because conspicuous coloration involves long-dis-
tance communication, background contrast and large patch size are
more important for conspicuousness than for distinctiveness. Complex
coloration (the juxtaposition of small, contrasting patches of color) is
an important component of distinctiveness, but not of conspicuousness.
Distinctive coloration may serve as a sign stimulus or as a social releaser
(Dilger, 1956; Colgan, 1983). When it is unclear whether conspicuous-
ness or distinctiveness is favored, we use the tern colorful to refer to
the two simultaneously.
Some color patches that appear at close range to be quite conspic-
uous are actually rather cryptic at a moderate distance (Hailman, 1977;
Endler, 1978). Thus, careful observation in the natural habitat is re-
quired before conspicuousness can be evaluated (Lythgoe, 1979; Burtt,
1986). Because cryptic coloration is the first line of defense against
predation for most animals (Endler, 1978; but see Hailman, 1977; Baker
and Parker, 1979), individuals may be selected for short-range distinc-
tiveness for communication with conspecifics and for long-range cryp-
sis for protection against predators. Certain patterns, such as the stripes
of zebras, achieve an excellent balance between distinctiveness and
crypsis (Endler, 1978).
When conspicuousness of plumage is favored for intraspecific com-

munication, a number of compromises may be favored because of the
color conflict (Hingston, 1933; Hamilton and Peterman, 1971; eott, 1985)
between communication and crypsis. Most authorities argue that the
benefit of crypsis is lessened visibility to predators (Endler, 1978, and
references cited therein), but a major benefit of crypsis might be less-
ened visibility or lessened threat to competitors. Morton (1976) attri-
butes the crypsis of young Yellow Warblers (Dendroica petechia) to
the fact that they must often intrude on areas defended by adults to
obtain food. Similarly, young hummingbirds lack the iridescent gorget
of adults perhaps because they must intrude on territories defended by
adults to feed; in support of this idea, young hummingbirds were shown
to be more successful at intruding than were adults (Ewald and Rohwer,
1980). In Harris' Sparrow (Zonotrichia querula), reduced threat rather
than reduced visibility is suggested as the function of the more cryptic
coloration of young birds because they were attacked less frequently
than adults in open areas on a per-encounter basis (Rohwer and Ewald,
1981).
One of the ways available to birds to compromise between con-
spicuousness and crypsis is dynamic coloration: iridescence, erectile
crests, air sacs, and coverable patches of color, such as the epaulets of
the Red-winged Blackbird (Agelaius phoeniceus). Dynamic coloration
may also be favored to increase flexibility in signaling; for instance, a
male Red-winged Blackbird may signal that he is an owner by exposing
his epaulets and that he is an intruder by covering his epaulets (Hansen
and Rohwer, 1986). Other compromises between crypsis and conspic-
uousness include the restriction of conspicuousness to particular parts
of the body (often the face, chest, wings, or tail, but rarely the back),
seasonal color dimorphism, and age- and sex-limited expression of
conspicuousness. In many species in which the cost of conspicuousness
is particularly great, animals may use other modes of communication
(especially vocalizations for birds) for the same purposes for which
other species use color. It is probably because of the color conflict that
it is often difficult to characterize species on the cryptic-conspicuous
axis.
Another reason for the difficulty in characterizing species on the
cryptic-conspicuous axis is the extreme difficulty in quantifying con-
spicuousness in natural settings (Hailman, 1977, 1979; Lythgoe, 1979;
Burtt, 1986). Quantification of conspicuousness requires determining
(1) the discriminatory abilities of the various observers of an animal,
(2) biologically relevant distances between the observers and the an-
imla, (3) the color properties of the environments in which the animal
is seen, (4) the color properties of the backgrounds against which the
animal is seen, and (5) the color properties of the animal itself. The
complexity is overwhelming. Endler (1978) suggests that birds have
visual acuity and color vision similar to that of humans (but see Chen
and Goldsmith, 1986, and references cited therein, most published after
Endler's paper). Burtt (1986) provides a rationale for starting with the
assumption that all diurnal terrestrial vertebrates have similar abilities
in visual discrimination; however, he points out important violations
of this assumption. For example, birds are sensitive to ultraviolet light
(Parrish et al., 1984; Chen and Goldsmith, 1986), but humans are not.
Faced with this complexity, biologists will differ in their approach.
Some will study the visual abilities of birds in the laboratory (Hailman,
1967; Parrish et al., 1984; Chen and Goldsmith, 1986). Some will at-
tempt quantitative studies of conspicuousness in nature (Hailman, 1979;
Burtt, 1986; Endler, 1987). Some will be satisfied for now with quali-
tative and general discussions of relative conspicuousness (this chapter,
and most of the papers cited herein). Many will decide that conspic-
uousness is too fuzzy a concept for them and will stop reading right
here. Despite the inherent difficulties in quantifying conspicuousness,
we believe that conspicuousness is the major factor that is selected for
or against in animal communication. We believe that progress in sen-
sory physiology concerning the visual discriminatory abilities of a va-
riety of animals, added to careful field observations of the visual context
within which animals are seen, will allow us to avoid or correct mis-
takes in our qualitative assessments of relative conspicuousness.
1.2. A Brief History of Color Hypotheses

New hypotheses concerning the adaptive significance of the col-
orfulness have appeared ever since Darwin's publication of The Descent
of Man, and Selection in Relation to Sex in 1871. Darwin wrote that
colorfulness and "ornaments of all kinds ... apparently serve to excite,
attract, or fascinate the females" (p. 394 of 2nd edition, 1890). Although
Darwin recognized that colorful males are subject to intense intrasexual
selection, he nonetheless maintained that the coloration itself serves
primarily to attract females. Wallace (1889) rejected Darwin's conten-
tion that colorfulness was due to female choice, believing, as did many
of Darwin's critics, that female choice of male colors implied an un-
acceptable "aesthetic sense" in animals. Instead, Wallace proposed that
colorfulness evolved to increase the distinctiveness of species-specific
coloration in order to prevent hybridization and to promote the dis-
CONSPICUOUS COLORA nON 57
covery of flocks by lost conspecifics. Moynihan (1960) expanded Wal-

lace's ideas on the uses of colorfulness by flocking birds.
Hingston (1933) rejected both sexual selection and species recog-
nition arguments and proposed that colorfulness was used in all cases
for warning (to potential predators) or threat (to potential rivals), often
failing to distinguish the two. Hingston also developed the idea of the
color conflict between crypsis and conspicuousness (see Section 1.1).
Huxley (1938) presented the first balanced review of the theories of
bird coloration, including a classification of the possible functions of
coloration that remains essentially complete today. Cott (1946; see also
Cott and Benson, 1970) extended the category of warning coloration
for birds by presenting evidence that many birds are unpalatable and
that colorfulness may be positively correlated with unpalatability. Baker
and Parker (1979) further extended the theory of warning coloration in
birds by suggesting that some birds are so vigilant and so agile that
they are unprofitable prey for most predators at most times and that
individuals that are relatively "unprofitable prey" signal this fact through
colorfulness.
2. THE THREE RULES OF AVIAN COLOR DIMORPHISM
Many intraspecific patterns of bird coloration have been described;

a number of these patterns are referred to in this chapter. Three of these
patterns recur in our work over and over again, and it is primarily these
patterns that we wish to be able to explain. We refer to them as the
three rules of avian color dimorphism. They are as follows:
1. When birds are sexually color dimorphic, males are more col-
orful than females.
2. When the age classes of birds feature different colors, adults are
more colorful than young birds.
3. When birds are seasonally color dimorphic, breeding season
birds are more colorful than nonbreeding season birds.
All three patterns of dimorphism have been documented for a va-
riety of species (Darwin, 1871), for waterfowl (Kear, 1970), for the Eu-
ropean avifauna (Baker and Parker, 1979), and for selected groups of
North and Central American passerines (Skutch, 1940). Sexual and
seasonal color dimorphisms have been documented for African plo-
ceids (Moreau, 1960; Crook, 1964) and for North and Central American
passerines (Skutch, 1957; Hamilton, 1961; Hamilton and Barth, 1962;
Bailey, 1978). In addition, Burley (1981) documented patterns of sexual
dimorphism in a number of flocking species, and Goodwin (1960) doc-

umented patterns of sexual color dimorphism in pigeons. Andersson
(1983, and references cited therein) documented patterns of seasonal
color dimorphism in ducks. Rohwer and Butcher (1988) documented
age-related color dimorphisms in North American passerines during
the nonbreeding and breeding seasons, including information on sea-
sonal changes. The latter added to the work of Rohwer et a1. (1980),
which concentrated on the breeding season.
There are exceptions to each of these rules. For example, in the
three species of phalaropes (genus Pha1aropus) and in the Painted Snipe
(Rostratu1a bengha1ensis). females are more colorful than males (Dar-
win, 1871). Associated with this reversal of colorfulness is a reversal
in the role of the sexes in courtship and parental care. In some species
of woodpeckers, young birds of both sexes have more colorful head
patches than do adults (Darwin, 1871). It is probably relevant that wood-
peckers nest in holes and therefore are relatively immune from pre-
dation while in the nest. Finally, in Brachyramphus murrelets (Marbled
and Kittlitz's), winter adults are a high-contrast black and white, whereas
summer adults are a cryptic mottled brown. In these species, unlike
most alcids, pairs form at sea in winter and nest as isolated pairs on
the ground or in trees in the summer.
When these three rules are considered in combination, they indi-
cate that some form of sexual selection must be one of the important
selection pressures favoring colorful birds (Darwin, 1871; contra Baker
and Parker, 1979). Three forms of sexual selection are commonly in-
voked to explain colorful birds: epigamic species recognition (finding
a mate of the proper species), agonistic sexual selection (intrasexual
competition over mates), and epigamic sexual selection (mate choice).
Given that it is during the breeding season that colorful birds are
likely to expose their nest and sedentary offspring to visually hunting
predators, it is particularly striking that breeding-season birds are more
likely to be conspicuous than nonbreeding-season birds (Andersson,
1983). Thus, it is during the season in which conspicuous coloration
should impose the highest cost that birds are most likely to be colorful.
In most species, males are under stronger sexual selection than are
females (Darwin, 1871; Trivers, 1972). consistent with the finding that
males are more likely to be conspicuous than females. Finally, young
birds are commonly assumed to be handicapped in breeding relative
to adults (Lack, 1954, 1966, 1968; Selander, 1965, 1972); the increased
likelihood that they will be cryptic may therefore be a method of either
compensating for these handicaps (Rohwer et a1., 1980; Lyon and Mont-
gomerie, 1986) or of increasing survival at the expense of reproduction
while young (Lack, 1954, 1966, 1968; Selander, 1965, 1972; Studd and
Robertson, 1985; Rohwer and Butcher, 1988), or both.
Baker and Parker (1979) document the validity of these three rules
for European birds, but they argue that the rules are consistent
with the idea that colorfulness evolved as a signal to predators. They
argue that males and adults are more likely to be vigilant against pred-
ators and to be able to escape attack than are females and young, hence
that males and adults should signal to predators (using conspicuous
coloration) that they represent unprofitable prey. Moreover, they argue
that all adult birds in temperate regions are more profitable in winter
than in summer, because (1) birds must spend more time looking for
food in winter than in summer, (2) there is less cover in winter than
in summer, (3) the predator has fewer alternatives in winter than in
summer, and (4) young birds become relatively more experienced in
late winter than they were in summer. Andersson (1983) counters that
the patterns of seasonal color dimorphism, in particular, do not favor
Baker and Parker's (1979) interpretation because seasonal color changes
are not timed to coincide with the presence or absence of inexperienced
young, but rather are timed to coincide with the presence or absence
of courtship. The best example is the eclipse plumage of male ducks:
in species with an eclipse plumage, the males become cryptic at exactly
the time when inexperienced offspring first appear. Males of species
with extensive early-winter courtship molt out of eclipse plumage ear-
lier than males in species with only spring courtship (Andersson, 1983).
3. THE THREE RULES AND THE THREAT HYPOTHESIS
The threat hypothesis argues that conspicuously colored individ-

uals have evolved because they are better at defending resources. How
colorfulness might work as a threat within a monomorphic class of
animals is discussed in Section 6.7. The status-signaling hypothesis is
a subset of the threat hypothesis that argues that differences in con-
spicuousness have evolved to signal differences in the ability of indi-
viduals to win agonistic contests (Rohwer, 1975, 1982). The status-
signaling hypothesis might explain the three rules of color dimorphism
as follows: (1) males are more colorful than females in the nonbreeding
season when they are larger than females and thus better fighters, or
when defense of resources is more important for males than for females;
(2) older birds are more colorful than younger birds because their greater
experience gives them greater fighting ability; and (3) breeding birds
are more colorful than nonbreeding birds because competition for mates
and breeding space is common during the breeding season and because
there is rarely any way to avoid competition and still achieve high
mating success. Balph et a1. (1979) and Whitfield (1987) argue that the
status-signaling hypothesis should be restricted to cases in which dif-
ferences in coloration signal differences in fighting ability within age
or sex classes; however, we argue here that the greatest power and value
of the status-signaling hypothesis may be its ability to explain why
some species advertise information about age or sex while other species
hide it.
Males dominate females during the nonbreeding season in 14 of
the 18 sexually color-dimorphic species for which we obtained infor-
mation; the data are equivocal in two species (Table I). In captive flocks
of Chaffinches (Fringilla coelebs), females dyed to resemble males im-
proved their status against both males and females, even though most
males remained dominant to the dyed females (Marler, 1955). In two
species, females dominated males, even though they are more cryptic
than males. In eight species, the sexes are the same color. Only 3 of
the 26 species have a prebreeding molt; thus, it is uncertain for most
of these species that their plumage is an adaptation to the nonbreeding
season. The association of dominance and conspicuous coloration in
this sample may merely reflect the frequency of male dominance and
of male conspicuousness in the sample.
We should note here the interesting article by S. M. Smith (1980)
that suggests that female dominance may be the rule within breeding
pairs. This suggestion, even if proved true, is not particularly relevant
to the status-signaling hypothesis. The threat hypothesis suggests that
coloration should be useful in deterring fights among relative strangers,
not among individuals with a long-term close relationship (e.g., mates
or neighbors).
Experiments on two bird species in which adult males and females
dominate first-year males and females during the nonbreeding season
are consistent with the status-signaling hypothesis. In both species,
adults are more colorful than first-year birds. Experimental manipu-
lations in White-crowned Sparrows (Zonotrichia leucophrys) showed
that first-year birds dyed to mimic adults rise in status to equal that of
adults; thus, the signal normally correlated with age (and thus status)
is believed independently of other cues of age or fighting ability (Par-
sons and Baptista, 1980; Fugle et al., 1984). Similarly, first-year Harris'
Sparrows dyed to mimic adult males were able to dominate all other
first-year birds in a flock of all first-year birds (Rohwer, 1985). Similar
experimental results on a variety of species or the demonstration that
TABLE I
Male versus Female Dominance during the Nonbreeding Season o . b
Dominant Color
Species' sex? dimorphic? Prebreeding molt? Field/aviary'? Reference
Dendrocopos (Picoides) pubescens Male Yes No Field Kilham (1974)
Dendrocinc1a fuliginosa Female No Field Willis (1972)
Zootheria (Ixoreus) naevia( us) Male Yes No ? Martin (1970)
Parus atricapillus Male No No Field Odum (1942); Glase (1973)
Parus carolinensis Male No No Field Dixon (1963)
Parus major Male Variable No Field Brian (1949)
Zosterops lateralis Male Yes ? Both Kikkawa (1961)
Zonotrichia (MelospizaJ melodia Male No No Field Knapton and Krebs (1976)
Zonotrichia querula Male Variable Yes Field Rohwer et a1. (1981)
Junco hyemalis Male Variable No Field Ketterson (1979)
Icterus spurius Male Yes No Field Butcher and Wimberger
(unpublished manuscript)
Fringilla coelebs Male Yes No Both Hinde (1956)
Fringilla montifringilla Male Yes No Both Hinde (1956)
Carduelis chloris Male Yes No Aviary Hinde (1956)
Carduelis tristis Male Yes Yes Both Coutlee (1967)
Curduelis carduelis Male No No Both Hinde (1956)
Acanthis (Carduelis) flammea Male Yes No Aviary Dilger (1960)
Carpodacus purpureus Female Yes No Both Samson (1977)
Carpodacus cassinii Female Yes No Both Samson (1977)
Carpodacus mexicanus For = Yes No Av/field Thompson (1960)
Loxia curvirostra Male Yes No Both Tordoff (1954)
Pyrrhula pyrrhula Female? Yes No Both Hinde (1956)
Coccothraustes coccothraustes Male Yes No Both Hinde (1956)
Coccothraustes vespertinus Male Yes No(sl?) Field Balph et al. (1979)
Cyanocitta stelleri Male No No Field J. L. Brown (1963)
Garrulus glandarius Male No Yes Aviary Goodwin (1951)
"Spring molt: Dwight (1900) and Forbush and May (1929) for eastern North America; Oberholser (1974) for western North America; Witherby et 01, (1943)
for England.
bPrebreeding molt: sl? refers to the possibility of a very restricted prebreeding molt. All prebreeding molts in this group are considered partial molts.
'Scientific names and sequence from Clements (1981), based on Morony et oJ. (1975); in parentheses, from A.O.V. (1983).
a large number of unusual color patterns are correlated with unusual

dominance patterns will be required to establish the generality of the
status-signaling hypothesis.
4. VARIABILITY, MONOMORPHISM, AND THE THREAT

HYPOTHESIS
Consistent with the three rules of avian color dimorphism is the

fact that, in many species, males and females are equally colorful, young
and adult birds are equally colorful, and/or breeding-season and non-
breeding-season adults are equally colorful. In these species, either
there must be a powerful constraint against color dimorphism, or there
must be selective pressures other than sexual selection that favor col-
orful birds. In addition, many species show within-class color varia-
bility. We argue that the importance of coloration for threat is most
consistent with the known patterns of the presence and absence of the
three color dimorphisms.
There are four major kinds of plumage variability within a bird
species: (1) no variability (all individuals either cryptic or conspicuous);
(2) between-class variability, with two to four more or less distinct color
classes; (3) within-class variability within one, some, or all classes; and
(4) variability unrelated to sex or age. For most of the species discussed
in this section, the plumage variability is correlated (at least to some
extent) with age and sex; for color polymorphisms that are independent
of age and sex, see Section 5. Plumage variability in birds is poorly
documented, with essentially no established methodology for quanti-
fication; thus, few species can be confidently assigned to the above four
categories.
A previous discussion (Rohwer, 1982) suggested that variable plu-
mages might be more characteristic of the nonbreeding season and that
monomorphic plumages might be more characteristic of the breeding
season. Nonetheless, examples of all four kinds of variability can be
found in both seasons; thus, the discussion of factors influencing which
pattern will characterize a species should address both seasons.
A major test of the status-signaling hypothesis is its ability to ac-
count for the four categories of plumage variability listed above.
4.1. Monomorphism
If the threat hypothesis is relevant, monomorphic cryptic species
should fall into one of four classes: (1) species for which aggression is
CONSPICUOUS COLORATION
unimportant; (2) species in which crypsis for avoiding predation is

more important than colorfulness for success at agonistic encounters;
(3) species that must sneak resources that are defended by more dom-
inant species; or (4) species for which coloration cannot facilitate win-
ning or reduce the number of aggressive encounters (see Section 6.7).
Monomorphic colorful species should be those in which all indi-
viduals must win agonistic contests to survive or reproduce. If a pop-
ulation can be divided into relatively good fighters and relatively poor
fighters, a major question might be: In what situations should (or can)
poor fighters disguise their lack of fighting ability? Poor fighters should
try to disguise their poor fighting ability when there are few avenues
to survival or reproductive success apart from winning fights. Poor
fighters may be able to disguise their poor fighting ability when contests
are often decided merely on the basis of priority (see Section 6.7) or
in other circumstances in which contestants are reluctant to fight, per-
haps because fighting is risky (Rohwer, 1982) (see Section 6.7). Because
both plumage and fighting ability are often correlated with age and sex,
plumage monomorphism may result when poor fighters (young birds,
birds of the subordinate sex, or other poor fighters) mimic the plumage
of good fighters in order to hide information about relative fighting
ability.
Poor fighters may not mimic good fighters because either (1) they
suffer less aggression by being cryptic or by identifying themselves as
subordinates, or (2) they can successfully obtain resources without fighting
dominants. Crypsis is a benefit to a poor fighter when he can sneak
resources defended by dominants (Ewald and Rohwer, 1980); subor-
dinates might suffer less aggression from a dominant than other dom-
inants would when dominants benefit from living in a group and prefer
subordinates as company because they provide less competition (Roh-
wer and Ewald, 1981).
4.2. Between-Class Variability

Between-class plumage variability might occur in two major situ-
ations under the threat hypothesis: (1) when one class of individuals
defends resources and other classes do not (Morton, 1976), and (2) when
individuals of the species live in groups (at least part of the time) and
there is a within-group dominance hierarchy (status signaling). These
situations may apply primarily to the nonbreeding season, but indi-
viduals of many species do not defend exclusive all-purpose territories
during the breeding season and may form groups at that time, especially
for foraging (Lyon and Montgomerie, 1986; Montgomerie and Lyon,

1986).
4.3. Within-Class Variability

A major unachieved goal is to explain why some variable species
have two color classes, some three, some four, while others are contin-
uously variable (both within and between classes). Two conditions may
favor continuous variability over discrete variability under the status-
signaling hypothesis: (1) a large amount of intraclass competition (Roh-
wer et 01., 1980; Rohwer, 1982), or (2) an uncertain environment, so
that individuals with intermediate fighting ability do not know whether
it would be better to signal dominance or subordinance at the time of
the molt (Rohwer, 1982).
A major unresolved issue in understanding continuously variable
species is whether or not plumage coloration is correlated with dom-
inance within age and sex classes. Some studies have found no cor-
relation within classes (Balph et 01., 1979; Watt, 1986a,b; Jackson et
01., 1988, contra Rohwer et 01., 1981). A study on Great Tits (Porus
major) (Jarvi and Bakken, 1984) showed that bib coloration was strongly
correlated with dominance within age and sex classes. In first-year male
Purple Martins (Progne subis), Rohwer and Niles (1979) found that birds
that were more like adult males dominated birds that were more like
females.
If dominance within age and sex classes is not correlated with
plumage differences, then the individual recognition hypothesis (Col-
lias, 1943; Shields, 1977; Whitfield, 1986, 1987) may be invoked to
explain why some species are continuously variable. The individual-
recognition hypothesis argues that some species are more variable than
others because individuals of those species use plumage variability to
remember the outcome of individual encounters. Thus, long-lasting
intransitive dominance relationships should be more common in con-
tinuously variable species than in less variable species. In other words,
dominance relationships in continuously variable species should be
more stable between two individuals (because of better memory of
individuals) and should be less linear in the flock as a whole (because
individuals can use individual rather than class cues to decide whether
they can defeat an individual). None of these predictions has been tested
to date. A final note: the individual-recognition hypothesis is unable
to explain why a color characteristic might be correlated with age and
sex class; thus, the status-signaling hypothesis may be useful even in
cases where within-class status is not correlated with plumage differ-

ences. The null hypothesis for the occurrence of continuous variability
is that it is an unselected by-product due to little or no selection for
monomorphism (Balph et 01., 1979).
5. COLOR DIMORPHISMS/POLYMORPHISMS
INDEPENDENT OF SEX, AGE, AND SEASON
A number of species of birds and other animals exhibit color di-

morphisms or polymorphisms independent of sex, age, and/or season.
Many of these involve melanism. In birds, these dimorphisms/poly-
morphisms are found in the families Procellariidae, Ardeidae, Accip-
itridae, Falconidae, Stercorariidae, Strigidae (Huxley, 1955), Cuculidae
(Payne, 1967), Laniidae (Hall et 01., 1966), and Emberizidae (Johnson
and Brush, 1972; Wunderle, 1981, 1983). To date, no generalizations
about the adaptive significance of these color patterns can be made. In
fact, in the case of the Snow Goose (Chen caerulescens), one research
group argues that there are no adaptive differences among blue, white,
or intermediate morphs (Rockwell et 01.,1985; Cooke et al., 1985; Find-
lay et 01., 1985).
If a color dimorphism/polymorphism is not selectively neutral, it
may be transitory because of the selective advantage of one color morph
compared with the other(s), or it may be stable as a result of frequency-
dependent selection or geographical differences in selective pressures.
Frequency dependence requires that each color morph be selectively
advantageous when rare relative to the equilibrium frequency at which
fitnesses are equal. When color polymorphisms are related to geograph-
ical differences, a morph-ratio cline may result. Frequency-dependent
selection for a color characteristic used in conspecific signaling has yet
to be demonstrated satisfactorily in any species, although opposing
selective pressures have been demonstrated in some and speculated
about in others.
For example, two fish polymorphisms are apparently maintained
by female preference for conspicuous morphs and by predation pressure
in favor of cryptic morphs (Semler, 1971; Moodie, 1972; Endler, 1980,
1983, 1987). Female Three-spined Sticklebacks (Gasterosteus aculea-
tus) prefer red males, perhaps because red males are better at defending
their eggs from conspecific predation (Semler, 1971). However, red
males suffer higher predation from other fish species (Moodie, 1972).
Female guppies (Poecilia reticu1ata) prefer conspicuous males with

many red and iridescent spots (Endler, 1980; Kodric-Brown, 1985) and
with large tails (Bischoff et a1., 1985). Two reasons have been proposed
for this preference. First, red spots contain carotenoids that must be
obtained in the diet; thus, red spots are an honest signal of foraging
ability (Endler, 1980; Kodric-Brown, 1985). Second, conspicuous males
are vulnerable to predation; thus, a living conspicuous male has proved
his ability to avoid predation (Endler, 1980; Bischoff et a1., 1985; Ko-
dric-Brown, 1985). On average, male guppies have fewer spots and
smaller tails in populations with more dangerous predatory fish (Endler,
1980; Endler in Bischoff et a1., 1985), indicating that predation selects
for crypsis in guppies.
Melanism often has correlated physiological effects (Ford, 1975;
Murton and Westwood, 1977; Borowski, 1981), which may lead to geo-
graphically related advantages of the morphs. There appear to be at
least three examples of this in birds. In the Rock Dove (Columba 1ivia),
melanic males breed earlier and for a longer period and are favored in
areas that support longer breeding seasons (Murton et a1., 1973). In
bananaquits (Coereba fJaveo1a), on the island of Grenada in the West
Indies, black morphs live in parts of the island with more rainfall and
spend more time in the shade than do the yellow-and-black morphs
(Wunderle, 1981). In Parasitic Jaegers (= Arctic Skuas) (Stercorarius
parasiticus), dark males have larger territories and are preferred as
mates by at least some females; light males breed at a younger age than
do dark males (O'Donald, 1980, and references cited therein). Given
these examples, one is tempted to predict important physiological dif-
ferences among dark ("blue") and light Snow Geese, but none has been
discovered in intensive studies (Cooke et a1., 1985; Findlay et a1., 1985;
Rockwell et a1., 1985).
In general, light ventral coloration is favored in aerial predators
because of its crypsis when viewed against the sky by terrestrial prey
(Mock, 1981; G6tmark, 1987; but see Kiltie, 1988). However, in many
species of raptors, there is a ventrally expressed dimorphism or poly-
morphism in coloration. The avoidance-image hypothesis (Paulson, 1973;
Rohwer, 1983; Rohwer and Paulson, 1987) suggests that potential prey
individuals of certain species may more consistently avoid predators
of the same color morph as one that has attacked them previously and
thus be more vulnerable to attack from a predator with a novel color
morpho Payne (1967) makes a parallel argument to explain the color
polymorphism of certain brood parasitic cuckoos. For hawks, four in-
direct tests support this hypothesis (Paulson, 1973; Rohwer and Paul-
son, 1987): (1) the color differences are primarily expressed ven-
trally,the side most apparent to potential prey; (2) the color differences
are more likely to be present in species whose diet includes prey species
that are more visually acute and are more likely to modify their behavior
based on experience; (3) migratory species of Buteo are more likely to
be color polymorphic than are resident species; and (4) among poly-
morphic species of Buteo, migrants usually occur in more than two
morphs and residents usually occur in two. A direct test of the avoid-
ance-image hypothesis has yet to be performed: the hypothesis predicts
that naive prey should be more readily captured by predators with light
venters, while prey that have been attacked by light predators should
be more readily captured by predators with dark venters (Rohwer, 1983;
Rohwer and Paulson, 1987).
Mock (1981) reviews a number of hypotheses that have been ad-
vanced to explain color differences within heron species. He presents
experimental data showing that more fish were trapped around models
of white herons than around models of dark herons when the models
were placed in clear, shallow water on sunny days where herons had
previously been seen foraging. These data support the argument that
white herons are more cryptic to prey viewing them against bright skies.
However, Caldwell (1986) suggests that dark herons may be more cryp-
tic to prey in other habitats. In addition, Caldwell (1986) showed that
more hawks were attracted to white herons than to dark herons in
Panama. Kushlan (1977) showed that white models of wading birds
placed in potential foraging areas attracted more individual wading
birds than did dark models. Thus, the balance between dark and light
coloration in wading birds may be determined by the relative benefits
of conspicuousness or crypsis to conspecifics, guild members, preda-
tors, and prey in a variety of habitats.
There are strong geographic differences in color-morph ratios in
some species (see Mock, 1981 and references cited therein). In three
species, Great Blue Heron (Ardea herodias), Grey Heron (A. cinerea),
and Reddish Egret (Egretta, Dichromanassa, or Hydranassa rufescens),
white morphs appear to predominate in areas in which the opportunity
for hunting in clear, open water with bright skies predominates. Sim-
ilarly, in Reef Herons (Egretta sacra), Holyoak (1973) found the light
morph to predominate in Polynesian islands with white coral beaches
and clear water. However, to what extent different color morphs dem-
onstrate microhabitat selection within a geographical area (Mock, 1981)
remains controversial; such selectivity would be expected if white her-
ons have a hunting advantage and a relative immunity to predation in
open water.
Unlike other herons, Little Blue Herons (Egretta. Florida. or Hy-
dranassa caerulea) show an age-related color dimorphism. Caldwell

(1981) has shown that the white immatures have a foraging advantage
over the dark adults in mixed-species flocks because they are attacked
less frequently than adults by the socially dominant Snowy Egret (Egretta
thula), a white species.
Although a number of studies have addressed the relative con-
spicuousness of dark and white morphs in wading birds, the physio-
logical hypotheses have yet to be tested in either wading birds or rap-
tors.
The case of the White-throated Sparrow (Zonotrichia albicollis)
may represent a bridge between those color dimorphisms that are and
those that are not sex related. The black-and-white-striped crowns of
adults are linked with the presence of one or more 2m chromosomes;
tan-and-brown-crowned adults have only 2 chromosomes (Thorney-
croft, 1975). In an aviary study, Watt et al. (1984) found that, on average,
black-and-white-crowned males had the highest social rank, followed
by tan-and-brown males and tan-and-brown females. Black-and-white-
crowned females had the lowest social rank. If these results are sup-
ported by further study, it suggests that black-and-white crown color-
ation is favored in adult males and that tan-and-brown crown coloration
is favored in adult females. These results suggest that a genetic linkage
between the color morphs and sex would rapidly spread to fixation if
introduced into the population.
Another major question that occurs in color differences that are
not sex related is that of assortative and disassortative mating. Non-
random mating of either type may indicate selection for optimal out-
breeding (Bateson, 1983), depending on the conditions. Assortative mating
has been shown in Snow Geese (Cooke and Davies, 1983; Findlay et
al., 1985) and in Parasitic Jaegers (= Arctic Skuas) (O'Donald et aI.,
1974; O'Donald, 1959). If assortative mating is an adaptive behavior,
individuals that mate with similar individuals should have greater re-
productive success than those that mate with dissimilar individuals;
however, in Snow Geese (Cooke and Davies, 1983; Findlay et aI., 1985),
there was no evidence of differential success of like and unlike pairs.
Cooke and Davies (1983) and Findlay et al., (1985) argue that assortative
mating is merely a consequence of imprinting and that imprinting func-
tions primarily to ensure conspecific matings. Disassortative mating
has been shown in White-throated Sparrows (Lowther, 1961), Rock
Doves (Murton et aI., 1973), and the fish genus Xiphophorus (Borowski,
1981). Disassortative mating may be favored when producing either
diverse or heterozygous young, or both, is favored. In disassortative
mating, imprinting for species recognition is not a confounding vari-
able; thus, it seems more likely to prove a behavioral adaptation in and

of itself.
6. CONTRASTING THE HYPOTHESES
The preceding sections suggest some of the broad patterns of bird

coloration that we seek to explain. It is clear that broad patterns of bird
coloration will continue to be interpreted in different ways, until more
decisive tests of individual hypotheses are available. Thus, we devote
the remainder of this chapter to proposing the kinds of evidence that
we believe should be collected to determine which hypotheses are most
likely to explain particular intraspecific and interspecific patterns. We
present the hypotheses in terms of dichotomous choices that can be
made in determining which hypotheses are most likely to apply. First,
we ask whether coloration serves a signaling function or a physiological
function. If coloration is a signal, we ask whether it is directed primarily
to conspecifics, to potential predators, or to potential prey. If coloration
is directed to conspecifics, we ask whether we can separate breeding-
season function from nonbreeding-season function. If coloration is a
signal of species identity, is it a signal to competitors (agonistic species
recognition) or to potential mates (epigamic species recognition)? If an
adaptation to the breeding season, is the coloration directed at potential
competitors (agonistic sexual selection) or at potential mates (epigamic
sexual selection)? If a signal to potential conspecific mates, is color-
fulness an object of mate choice or of attraction? If females choose males
on the basis of their coloration, what benefit might they derive? If
females are passively attracted to males based on their coloration, are
they attracted to conspicuous males, or are they attracted to males with
an arbitrary patch of color? If a signal to potential conspecific compet-
itors, is it a signal of quality (fighting-ability hypothesis) or presence
(priority hypothesis)?
6.1. Physiology or Communication

Does the coloration have a physiological or a communicative func-
tion? This is the first of many dichotomies that may often produce the
answer "both." Given that a communicative function favors a conspic-
uous or distinctive coloration, which color is employed for that function
may well be determined by the physiological properties of the colors.
Most of the studies on the physiological properties of colors have
concentrated on black or white (Hamilton, 1973; Hailman, 1977; Wals-
berg et al., 1978; Burtt, 1979, 1981, 1986). Most of the sexual, seasonal,
and age-related color differences that we hope to explain are between
colorful (black, white, or bright hues) and cryptic (brown, gray, or olive).
Unfortunately, the above studies do not contrast the physiological dif-
ferences between black or white individuals and cryptic individuals.
A major exception is Walsberg's (1982) paper on sexual color dimorph-
ism in the Phainopepla (Phainopepla nitens). He demonstrated that the
difference in radiative heat load due to the difference between the black
male plumage and the gray female plumage was minor compared with
the differences in heat load that could be achieved in other ways (e.g.,
changes in orientation); in addition, Walsberg found that, under similar
conditions, the black males suffered a higher heat load than did the
gray females. In contrast to the expectations of Walsberg et a1. (1978),
black males had a higher heat load even in high wind conditions.
Therefore, he attributes the sexual color dimorphism to signaling re-
quirements. Given that the Phainopepla lives in the hot, arid desert of
the southwestern United States, Walsberg's result may prove to be gen-
eral for thermal colors, and in general, the all-black coloration of desert
birds may be suboptimal in the heat of the day. All-black coloration in
desert birds may be favored because it increases conspicuousness in
signaling situations or because the melanin in black feathers effectively
reduces feather abrasion from blowing sand (Burtt, 1986).
A number of physiological functions might be served by particular
colors or patterns, including improving vision, promoting optimal heat
or water balance, providing mechanical protection against abrasion,
and providing a shield against ultraviolet radiation. If analysis suggests
that a color pattern may be favored because of its physiological effects,
see the papers cited in this section (Burtt, 1981, 1986, are the most
convenient entries into this literature). For the remainder of the review,
noncryptic coloration is assumed to function as a signal.
6.2. Signaling to Conspecifics, Predators, or Prey

If coloration is used for communication, it is aimed at conspecifics,
at potential predators, or at potential prey? Most students of bird co-
loration have argued that colorfulness is a signal to conspecifics and
that the major cost of conspicuousness is increased vulnerability to
predation (Endler, 1978, and references cited therein). However, the
warning hypotheses argue that colorfulness evolved to signal to pred-
ators that colorful individuals are undesirable prey items (Cott, 1946;
Cott and Benson, 1970; Baker and Parker, 1979). Thus, the two classes
TABLE II
Parental Care in Monomorphic Species versus Dimorphic Species
Parental care"
Both sexes Female alone
Monomorphism 18
Dimorphism 58
"The association between sexual color monomorphism and biparental care in waterfowl (Kear, 1970).
"Numbers refer to individual species. However, almost all the monomorphic species are more closely
related to each other than they are to the dimorphic species. Thus, the association between mono-
morphism and biparental care in waterfowl might be best considered just one data point.
of hypotheses appear to make diametrically opposed predictions con-

cerning the association of conspicuousness and predation rate.
6.2,1. Are Conspicuous or Cryptic Birds More Vulnerable to

Predation?
We can think of three possible ways to test the question: are con-
spicuous or cryptic birds more vulnerable to predation?
1. Compare the vulnerability to predation of cryptic and conspic-
uous classes of birds: Baker and Parker (1979; see also Baker and Houn-
some, 1983; Baker, 1985) made an excellent case that many of the
interspecific differences in coloration can be explained by differences
in vulnerability to predation, with the more vulnerable species being
more cryptic, Specifically, they found the following patterns: (1) species
that live on the ground or on the water are less colorful and more
sexually color dimorphic than other species; (2) adults of smaller spe-
cies are less colorful and more dimorphic than adults of larger species;
(3) species with exposed nests are less colorful than species with con-
cealed nests; and (4) classes of birds that provide more parental care
are less colorful than classes of birds that provide less parental care.
Two other large interspecific surveys of sexual color dimorphism and
monomorphism, in ducks and in North American passerines, also sug-
gest that vulnerability to predation may be responsible for many of the
patterns of occurrence of conspicuous coloration. Kear (1970) found
that in most monomorphic species of waterfowl (which, in general, are
not gaudily colored), both sexes shared parental duties, whereas in most
dimorphic species (having, in general, highly colorful males), females
raised the young alone (Table II). Most male passerines in North Amer-
ica feed their young. However, males of monomorphic species are much
TABLE III
Incubation of Eggs by Males of Monomorphic and Dimorphic Species
Male
incubation°
Yes No
Monomorphism 24
Dimorphism 27
"North American passerines, association at the species level between sexual color dimorphism and
male incubation of eggs (Verner and Willson, 1969).
bNumbers refer to individual species. However, a comparative analysis using known phylogenies of
the included species has not yet been done, thus the biological persuasiveness of this correlation
has not yet been established.
more likely to incubate eggs than are males of dimorphic species (Table
III) (Verner and Willson, 1969). These results indicate that presence at
the nest selects strongly for crypsis. However, the intenstiy of sexual
selection on males is inversely proportional to the extent of male pa-
rental care (Trivers, 1972; Murton and Westwood, 1977), and differ-
ences in the relative intensity of sexual selection on the two sexes may
explain these two patterns of sexual color dimorphism and mono-
morphism.
2. Compare annual predation rates on banded (ringed) birds: Baker
and Hounsome (1983) compared 14 species of passerine birds (includ-
ing both sexes of four sexually color dimorphic species) and found that
conspicuous birds were less likely to be preyed on than cryptic birds.
Unfortunately, their sample size was small (and poorly defined).
3. Compare the proportion of cryptic and conspicuous individuals
in the diet of predators that feed on dimorphic prey with the proportion
available in the foraging areas of the predator (e.g., by studying remains
at a hacking site of cache of a predatory bird): In the springtime in
Iceland, conspicuously white male Rock Ptarmigan (Lagopus mutus)
suffer higher predation from Gyrfalcons (Falco rusticolus) than do the
cryptic brown females (Gardarsson, 1971, cited in Lyon and Montgo-
merie, 1985; O. Nielson, personal communication).
Despite the apparent promise of these three tests, "sexual selection
theory makes no particular prediction about the relation between pre-
dation rate and conspicuousness among species" (Lyon and Montgo-
merie, 1985), especially if interspecific risk of predation varies for rea-
sons other than conspicuousness, as is likely (Lyon and Montgomerie,
1985, see also Krebs, 1979). Each of these three proposed tests suffers
from the fact that a number of factors could produce a bias of individuals
in the diet of a predator. As with any correlative study, cause and effect
are unclear. Results of any of the three tests could be consistent both
with the idea that conspicuousness advertises the unprofitability of
potential prey and with the idea that sexual selection favors more con-
spicuous individuals when predation costs are low. Clearly, what needs
to be tested is whether predators decide not to pursue certain classes
of individuals because of their conspicuous coloration. Thus, a different
approach is needed.
6.2.2. Do Predators Prefer Cryptic Prey?

The most direct way to study the warning hypotheses of Cott (1946)
and Baker and Parker (1979) is to examine the actual choices between
conspicuous and cryptic prey made by predators. This could be done
by following domestic animals (e.g., cats), radio-tagged predators, or
perhaps trained raptors. An experimenter could offer the predators a
series of choices between two potential prey items: one cryptic and one
conspicuous. Since individual predators may form search images for
particular prey types (Croze, 1970; Curio, 1976), such a study should
include a number of individual predators, with a significant number
of prey items per individual predator. The warning hypotheses predict
that predators should consistently refuse to chase conspicuous indi-
viduals.
A second important test is to compare the success rate of predators
trained to chase conspicuous birds and those trained to chase cryptic
birds. This would test Baker and Parker's (1979) idea that conspicuous
individuals ought to be more difficult to capture than cryptic individ-
uals.
6.2.3. To Whom Is a Signal Directed?

Another major way to distinguish between signaling to predators
or to conspecifics is to study the context of a signal (i.e., who is present
when the signal is given and to whom the signal is directed). This can
best be done with dynamic coloration or coloration that is restricted to
a particular part of the body. For example, male Red-winged Blackbirds
(Agelaius phoeniceus) expose their epaulets to conspecific males and
females during the breeding season when they are on their own territory
(Orians and Christman, 1968). When dangerous predators are present
nearby, when they forage away from their breeding territory, when they
intrude on occupied territories, and during the nonbreeding season,
male Red-wings cover their epaulets. Thus, both agonistic and epigamic
sexual selection seem relevant to the evolution of red epaulets, but
signaling to predators cannot apply.
Many birds have distinctive patches of color on their face, throat,
or breast. We believe that the most reasonable explanation for this
restriction of color is that the color is favored for signaling to conspe-
cifics and that it is restricted to lower the probability that it will be
seen by predators.
Another example is the phenomenon of dynamic or flash coloration
on the wings and tails of birds. Moynihan (1960) argues that these
patches are directed at flockmates and function to coordinate the takeoff
and flight of flocking birds. Baker and Parker (1979) argue that flash
coloration is directed at predators as either (1) protean defense, or (2)
perception advertisement. Hailman (1960) and others (Selander and
Hunter, 1960; Monroe, 1964) reported that flash coloration of the wings
was directed at potential prey and was used to flush prey items. Finally,
Burtt (1986) argues that flash coloration is directed at conspecifics in
the courtship displays of warblers. Baker and Parker (1979) found that
in European birds the presence of flash coloration on the upper surface
is correlated with small size and the amount of time spent on the ground
or in the water. Both are indications of vulnerability to predation and
are consistent with their unprofitable prey hypothesis. However, Baker
and Parker also found a correlation between flash coloration and non-
breeding gregariousness, as predicted by the flash-synchronization hy-
pothesis (Moynihan, 1960). The best resolution of these conflicting
hypotheses may be to observe the use of these patches in nature care-
fully, concentrating on what classes of animals are present when these
colors are flashed and how they behave. Experimentally obliterating
the patches and observing subsequent behavior and response should
also prove quite feasible.
The distinction between signaling to predators or to conspecifics
also needs to be made in studies of the function of conspicuous rump
patches in ungulates (Harvey and Greenwood, 1978, and references
cited therein). The major way to decide this question is to determine
which class of individuals is most likely to view the conspicuous rump
patch and to determine how the two classes of individuals respond
when they do see the rump patch. Similar questions can be asked of
the stotting behavior of ungulates and of the alarm calls of birds and
other animals (Harvey and Greenwood, 1978; Caro, 1986).
Surprisingly to us, Baker and Parker (1979) rejected the reasoning
that if a signal is used in an epigamic context epigamic sexual selection
is most likely to account for its evolution. Baker and Parker (1979)
argued as follows:
When some feature of male plumage is used during solitary courtship dis-
play to a female and is concealed or less conspicuous at other times ... ,
the possibility that the feature evolved through sexual selection might seem
greater than when a feature is continuously visible. Even here, however,
the possibility that the feature evolved initially in response to predation-
risk pressures requires consideration .... The critical factor seems likely to
be whether a displaying male represents a profitable or unprofitable prey
to a predator.
We believe that Baker and Parker's argument here is untenable. If a

color pattern is displayed only to females, the rational deduction is
that male-female communication produces the important selection
pressure favoring that color pattern. Similarly, if a color pattern is
displayed only to predators, predator-prey communication is the most
likely selection pressure favoring the color pattern. Many color patches
are displayed in more than one situation, making conclusions less
straightforward.
If these sorts of analyses indicate that communication between
potential prey and predators might be important for the evolution of
certain types of bird coloration, then we refer you to the cited references
and to Hailman (1977). For the remainder of this chapter, we assume
that signaling to conspecifics (or to ecologically similar or closely re-
lated species) is the function of colorfulness.
6.3. Breeding or Nonbreeding Adaptation

If a signal to conspecifics, is coloration an adaptation to the breed-
ing or to the nonbreeding season? The major question we wish to ad-
dress here is whether we can assume that the coloration that charac-
terizes an individual in one season is independent of the selection
pressures on the individual's coloration during another season. For
those bird species with two molts a year, the answer is unequivocally
yes. Unfortunately, many species of birds do not feature two molts a
year.
Molt is an energetically costly event. Studies of the energetic cost
of postnuptial molts show that the basal metabolic rate is elevated
20-40% for the duration of the molt, typically 3-6 weeks (King, 1980;
Walsberg, 1983). It may be that the cost of two molts a year is sufficiently
high to override any benefit that some birds might achieve by producing
different plumages for different seasons. On the other hand, it may be
that the species that require different plumages are precisely those that
molt twice a year. (Some species molt twice a year without changing
color, indicating that a twice-a-year molt can be favored for other rea-
sons, presumably high feather wear.)
There is a second method (in addition to two molts a year) to
produce plumage independence: feather tipping and feather abrasion
(Darwin, 1871). Almost all birds molt after breeding, and almost all
seasonally dimorphic species are more cryptic during the nonbreeding
season than during the breeding season. A number of birds have cryptic
tips on their new feathers that wear away with time (e.g., the European
Starling and the Snow Bunting). However, most of the species that we
know lack a spring molt do not look dramatically different in spring
than in fall, because the cryptic tips are narrow. Thus, there may be a
constraint on the ability of feather tips to produce a dramatically dif-
ferent plumage in two seasons. Further research into feather abrasion
and spring molts is critical to our understanding of seasonal indepen-
dence. Burtt's (1986) technique of experimental abrasion should facil-
itate studies of feather tips.
A lot of evidence suggests that colorfulness is more important dur-
ing the breeding season than during the nonbreeding season. First,
species that are seasonally color dimorphic are more conspicuous dur-
ing the breeding season than during the nonbreeding season-the third
rule of avian color dimorphism. Second, a reversal of sex role during
the breeding season results in reversed sexual color dimorphism (Le.,
in phalaropes and the Painted Snipe). Third, colorfulness is positively
correlated with polygyny in the European avifauna (Baker and Parker,
1979), and extravagant plumage (colorfulness plus elaborate and elon-
gated feathers) is positively correlated with promiscuity/polygyny in
the Birds of Paradise (LeCroy, 1981) (Table IV).
If plumage is not seasonally independent and if sexual selection
is a major selective pressure favoring colorfulness, older birds might
be expected to be colorful year-round and younger birds cryptic year-
round. This expectation follows from the assumption that the proba-
bility of reproductive success increases with age and experience (Lack,
1954,1966,1968; Studd and Robertson, 1985) and, therefore, that older
birds should maximize their reproductive success despite some cost to
survival, whereas younger birds should maximize their survival at some
cost to reproductive success. The pattern of age dimorphism is con-
sistent with the unprofitable prey hypothesis as long as younger birds
are more vulnerable to predators than older birds. Thus, if sexual se-
lection is a major selective pressure favoring conspicuousness and if
plumage is not seasonally independent, older birds may be more con-
TABLE IV
Polygyny and Dimorphism and Polygyny and Elaborate Plumage in Birds of
Paradise
Sexually Males with

Mating system/ color elaborate
species dimorphic? plumes?
Monogamous (presumed or known)

Macgregoria pulchra (known) No No
Lycocorax pyrrhopterus (presumed) No No
Manucodia
ater (known) No No
jobiensis (presumed) No No
chalybatus (known) No No
comrii (presumed) No No
Phonygammus keraudrenii No Two plumes
(known)
Paradigalla
carunculata (presumed) No No
brevicauda (presumed) No No
Promiscuous (male dispersion")

Semioptera wallacei (TU) Yes Yes
Orepanornis albertisi (OT) Yes Yes
Astrapia stephaniae (TL) Yes Yes
Parotia
sefilata (EL) Yes Yes
carolae (EL) Yes Yes
lawesii (EL) Yes Yes
wahnesi (EL) Yes Yes
Pteridophora alberti (EL) Yes Yes
Cicinnurus regius (EL) Yes Yes
Oiphyllodes magnificus (ONT) Yes Yes
Paradisaea
apoda (TL) Yes Yes
raggiana (TL) Yes Yes
minor (TL) Yes Yes
decora (EL) Yes Yes
rubra (TL) Yes Yes
guilielmi (TL) Yes Yes
Resource-defense polygyny
Epimachus mcyeri (OT) Yes Yes
Lophorina superba (OT) Yes Yes
Unknown
Loria loriae Yes No
Loboparadisea scricca No No
Cnemophilus macgregorii Yes One plume
(continued)
Table IV (Continued)
Sexually Males with
Mating system/ color elaborate
species dimorphic? plumes?
Ptilorus
paradiseus Yes No
victoriae Yes No
magnificus Yes No
Seleucidis melanoleuca Yes Yes
Drepanornis bruijinii Yes Yes
Epimachus fastuosus Yes Yes
Astrapia
nigra Yes Yes
splendidissima Yes No
mayeri Yes Yes
rothschildi Yes Yes
Diphyllodes respublica Yes Yes
Paradisea rudolphi Yes Yes
"Taxonomy from Morony et al. (1975).

bOata from Gilliard (1969), LeCroy (1981). Beehler (1983), and Beehler and Pruett-Jones (1983).
'The monogamous and unadorned species are all believed to be more closely related to each other
than to the other species. Thus. the data presented above are best considered to provide merely one
data point in support of a correlation between extravagant plumage and a promiscuous mating system.
dMale dispersion: TL. true lek; EL. expoloded lek; OT. dispersed territorial; ONT. dispersed nonter-
rilorial.
spicuous than would be adaptive in the nonbreeding season and youn-

ger birds may be more cryptic than would be adaptive in the breeding
season. If these predictions are true, we should be able to demonstrate
costs (in terms of predation or competition) of adult male conspicu-
ousness in the nonbreeding season and costs (in terms of reproductive
success) of young male crypsis in the breeding season. Correlative evi-
dence of the latter cost is beginning to appear, in that more conspicuous
first-year males have higher mating success than less conspicuous first-
year males in Indigo Buntings (Payne, 1982) and Black-headed Gros-
beaks (Hill, 1988) and perhaps in Pied Flycatchers (R0skaft and Jiirvi,
1983) and Darwin's Finches (Price, 1984). However, there are no ex-
perimental tests that prove that coloration is the cause of the higher
mating success (Baker, 1985).
Additional evidence that more cryptic young males are handi-
capped in breeding relative to more colorful young males is the fact
that, in three species, first-year males continue to molt in spring for up
to a month after arriving on the breeding grounds while adult males
are initiating breeding, suggesting that acquiring adult-male-like color-
ation is more important to them than is early breeding (American Red-

start: Rohwer et aI., 1983; Indigo Bunting: Rohwer, 1986; "Baltimore"
Oriole: S. Rohwer and Manning, unpublished data).
If a species exhibits two molts per year, suggesting that plumage
coloration in winter and summer is independent, then winter may be
the preferred season for studying the adaptive significance of conspic-
uous coloration, because there are fewer competing hypotheses in win-
ter. The hypotheses that seem most relevant to winter include threat,
especially status signaling (Sections 4, 5, and 6.7). signaling within
flocks (Section 6.2.3). agonistic species recognition (Section 6.4)' or
signaling to predators or prey (Section 6.2). Most of the discussion that
follows assumes that conspicuous coloration is adaptive in the breeding
season.
6.4. Agonistic or Epigamic Species Recognition

Is coloration a signal of species identity? If so, is it a signal to
potential mates (epigamic species recognition) or to potential compet-
itors (agonistic species recognition)? The species-recognition hy-
potheses are different from most of the other hypotheses we consider
in that they primarily predict interspecific differences in coloration.
The null hypothesis to all adaptive explanations of color differences
among species is that color differences among species arise due to
random genetic drift. There are at least three selective alternatives to
the species-recognition hypothesis. First, color differences among spe-
cies might accumulate in allopatry as a result of selection pressures for
optimal conspicuousness in different environments (Hailman, 1977).
Second, color differences within a species might spread rapidly because
of an evolutionary "arms race" (Dawkins and Krebs, 1979) between
good and poor fighters (Rohwer, 1982; West-Eberhard, 1983; Weldon
and Burghardt, 1984). Under this scenario, good fighters benefit by
looking different from poor fighters and poor fighters benefit by looking
the same as good fighters. The outcome of such an arms race is prob-
lematic (see Section 6.7); nonetheless, it provides a powerful mecha-
nism for generating dramatic color differences between species (Roh-
wer, 1982; West-Eberhard, 1983; Weldon and Burghardt, 1984). Such
a mechanism might be responsible for "leapfrog" patterns of color dif-
ferences (Remsen, 1984). Third, color differences between species might
develop rapidly because of the "runaway" process of nonrandom mat-
ing (Fisher, 1930; see also Section 6.6).
There are two species-recognition hypotheses. The epigamic ver-
sion argues that species color differences evolved as premating isolating
mechanisms to prevent interspecific hybridization (Dobzhansky, 1937;

Mayr, 1942, 1965). The agonistic version argues that species color dif-
ferences evolved to prevent erroneous interspecific aggression (the "poster
color" hypothesis proposed by Lorenz, 1962, 1966) in either the breed-
ing or nonbreeding season.
Naturalists have difficulty in assessing arguments that a particular
characteristic is selectively favored because it facilitates species rec-
ognition. On the one hand, we know that many birds are capable of
fine distinctions among individuals (stranger-neighbor discrimination
in bird song; parent-offspring recognition through simple calls; stable
dominance relationships within flocks), and therefore we assume that
species recognition ought to be automatic, using whatever differences
already exist. On the other hand, we know that interspecific hybrid-
ization does occur (although we rarely know the circumstances), and
we know that birds often respond to minimal stimuli (models, feather
tufts, red spots) as though they were conspecifics. In addition, the re-
sults of numerous studies are consistent with the interpretation that a
particular song, display, or color pattern is used for species discrimi-
nation (McKaye et al., 1984; Pierotti, 1987). However, no studies have
shown that these characteristics originated because of their function as
a species identity badge (but see Burley, 1986). Finally, we have the
twin problems that specific characteristics are often redundant (E. E.
Williams and Rand, 1977), or they may be completely absent (mor-
phological sibling species). Clearly, what is needed is to examine many
species that face different species-recognition problems to look for pat-
terns in the occurrence and redundancy of characteristics that may
serve as isolating mechanisms.
In its most general form, the epigamic species-recognition hypoth-
esis may apply to all bird species. However, another form of the ar-
gument applies only to some species. Mate recognition may be innate
or learned through sexual imprinting on a caregiving individual during
a sensitive period early in life (Hailman, 1959; Immelman, 1972; Colgan,
1983). Fine distinctions among species of very similar plumage can be
learned through sexual imprinting (Schutz, 1965). Immelman (1975)
argues that males that do not care for the young (and therefore are
unavailable for imprinting) need to be distinctive to permit innate mate
recognition.
Immelman's argument that species that rely on innate mate rec-
ognition are those that are distinctively colored cannot apply to most
passerine birds. Many conspicuously colored male and female passer-
ines feed both nestlings and fledglings and are available for sexual
imprinting. However, the argument may apply to ducks (Sibley, 1957;
Schutz, 1965) and to many promiscuous or polygynous species in which

males are more conspicuous than females and do not care for their
offspring.
To argue that a particular color pattern originated because it facil-
itated species recognition is to argue that the color pattern originated
either (1) after secondary contact with a potentially hybridizing species
(usually a closely related congener) in a situation where hybrids are
selected against (epigamic species recognition: Remington 1968), or (2)
after contact with an unrelated aggressive species of very similar size
and form in a situation where interspecific aggression is maladaptive
(agonistic species recognition). When two populations come into con-
tact, there will be some variability within the populations. Under the
epigamic hypothesis, females that prefer males that are most distinct
from the other species will be favored, as will the males that are most
distinct. Under the agonistic hypothesis, individuals that do not fight
the other species will be favored, and individuals that are more distinct
from the other species will suffer less aggression.
The recognition badge will be selected for as long as two potentially
hybridizing and aggressing species remain in syntopy and as long as
hybridization and interspecific aggression are selected against. The spe-
cies recognition badge is an ideal system for the evolution of runaway
sexual selection (Fisher, 1930). Under the epigamic version, any in-
crease in male divergence from the other species might allow females
to choose conspecific mates faster and with fewer errors. Thus, females
might be selected to prefer extreme males, and males might be selected
to be extreme. Under the agonistic version, any increase in color di-
vergence might lower the probability of erroneous aggression. The result
could be males that are much more divergent from their syntopic con-
geners than is necessary to avoid interspecific hybridization or aggres-
sion.
If the above reasoning is valid, color character divergence should
be common where two congeners overlap, especially in areas of sec-
ondary contact. It is in areas of overlap that hybridization or aggression
will occur and provide the selective pressure for developing the specific
differences in plumage that prevent erroneous mating or fights (ac-
cording to the species-recognition hypotheses). Thus, color differences
between species should originate in areas of overlap. Whether such
differences spread throughout the range of the species will depend on
rates of gene flow and selection pressures outside the area of sympatry.
In contrast to the prediction, color character divergence is sur-
prisingly rare (Rohwer et 01., 1980). When it has been found, the di-
vergent characters often have been quite minor: eye-patch in nuthatches
(Grant, 1975), eye-ring and iris color in gulls (N. G. Smith, 1966, but
see Pierotti, 1987), throat color in partridges (Watson, 1962), epaulet
color in blackbirds (Hardy and Dickerman, 1965; Hardy, 1967; Orians
and Christman, 1968), and iris color in grackles (Peterson, 1980). Pied
Flycatchers (Ficedula hypoleuca) provide a more interesting case: where
they overlap the range of the dominant Collared Flycatcher (Ficedula
collaris), males are browner and more femalelike than in other parts of
their range (R0skaft et aI., 1986). The general failure of the prediction
of character displacement suggests that most color differences between
species were developed in allopatry as a result of genetic drift or dif-
ferential selection pressures and were not developed in sympatry as a
result of selection for improved premating reproductive isolation. This
latter selection might operate by favoring individuals that are better
able to discriminate color differences that evolved in allopatry (' 'reinforce-
ment"), but even this process is in great dispute (Butlin, 1987).
A second prediction that follows from both species-recognition
hypotheses is that syntopic congeners or family members should be
more different from each other in coloration than are allopatric con-
geners or family members. According to this prediction, sibling species
should not be syntopic or, if they are, other behavioral isolating mech-
anisms should be present. In support of the prediction, Hamilton (1973)
found that the complexity of coloration in a group of Indian Ocean reef
fish increased as the number of potentially sympatric species belonging
to the same family increased. This correlation did not work at the
generic level even though in theory, the closer the relationship, the
stronger the trend should be.
Much of the support for the species-recognition hypotheses derives
from the observations that (1) islands rarely support more than one
congener, and (2) birds on islands are often less conspicuous than their
mainland congeners (Mayr, 1942, 1972; Sibley, 1957; Grant, 1965; Mo-
reau, 1966; Lack, 1970). However, island birds may also be more con-
spicuous than their mainland counterparts (e.g., females of the genera
Petroica and Pachycephala in the southwest Pacific (Mayr, 1942) and
female Red-winged Blackbirds (Agelaius phoeniceus) on Cuba and Puerto
Rico (Ricklefs and Cox, 1972). In addition, other hypotheses may be
consistent with the patterns of plumage differences between island and
mainland birds (Selander, 1965; Zahavi, 1981; Baker and Hounsome,
1983).
The epigamic version of the species-recognition hypothesis pre-
dicts that individuals that more closely resemble syntopic congeners
than normal adults should be handicapped in getting a mate. However,
two lines of evidence suggest that birds that deviate from species-spe-
cific plumage still are able to breed. In a number of bird species, males
breed in a sub adult plumage that is much less distinctive than the adult
male pluamge (see Rohwer et al., 1980, for North American passerines).
In addition, males of three species underwent dramatic color manip-
ulations but were still able to breed: (1) male Red-winged Blackbirds
whose epaulets were blackened so that they closely resembled Rusty
Blackbirds (Euphagus carolinus) or Brewer's Blackbirds (Euphagus
cyanocephalus) were capable of attracting conspecific mates and suc-
cessfully breeding if they were able to defend their territories (Smith,
1972); (2) male Common Yellowthroats (Geothlypis trichas) whose black
face mask was obscured were able to attract females on the same sched-
ule as were controls (Lewis, 1972); and (3) male "Bullock's" Orioles
(Icterus galbula bullockii) whose black coloration was bleached to orange
were able to attract females on the same schedule as were controls
(Butcher, 1984).
These experiments demonstrate that a dramatic change in colora-
tion may cause little problem for mate attraction. The Red-winged
Blackbird study is the most relevant, since the males were made to look
like syntopic congeners; however, it is less than definitive for two rea-
sons: (1) Peek (1972) found that his males with dyed epaulets were
unable to attract females until the dye wore off, and (2) Smith (1972)
did not compare harem sizes of experimentals and controls, even though
Red-winged Balckbirds are polygynous.
The agonistic version of the species-recognition hypothesis pre-
dicts that colorful animals should be aggressive and that intraspecific
aggression should be more common than interspecific aggression. Lor-
enz (1962, 1966) found support for both points in Caribbean coral reef
fish. Zumpe (1965) studied the behavior of eight species of conspicuous
butterfly fish (Chaetodontidae) in an aquarium and found that intra-
specific aggression was much more frequent and intense than inter-
specific aggression. In addition, she found that interspecific aggression
was often directed toward a heterospecific that was most similar in
coloration to the aggressor. Ehrlich et a1. (1977) rejected the conspecific
aggression hypothesis for coral reef fish because (1) they found no
correlation between conspicuous coloration and territoriality in coral
reef fish, and (2) when the fish they studied (Chaetodontidae) were
aggressive, they fought both heterospecifics and conspecifics. No sim-
ilar studies to these just mentioned have been performed on birds.
6.5. Agonistic or Epigamic Sexual Selection

If an adaptation to the breeding season, is the coloration directed
at potential competitors (agonistic sexual selection) or at potential
mates (epigamic sexual selection)? Students of bird song have tried to
distinguish between agonistic and epigamic functions; the answer in

many cases is that the two functions cannot be distinguished. If bird
song, which can be readily turned off and on in specific situations,
cannot be assigned an epigamic or agonistic function, it seems unlikely
that bird coloration can be assigned one or the other function. There
are a number of reasons to believe that the two functions will often be
inextricably linked. If advertising is the function of coloration or song,
mate advertising and territorial advertising are perfectly compatible
behaviors. If coloration is linked with high genetic quality, both male
and female conspecifics will benefit from using the information.
Nonetheless, there may be a number of cases in which an epigamic
or agonistic function can be assumed over the other. If a color patch is
usually displayed only to one of the sexes, communication to that sex
is the function of the coloration. If agonistic contests occur before mat-
ing occurs, the relative importance can be estimated using a modifi-
caation of techniques advocated by Arnold and Wade (1984).
Male Red-winged Blackbirds display their epaulets both to males
and to females (Orians and Christman, 1968). In two studies in which
the epaulets of territorial males were dyed black (Peek, 1972; Smith,
1972), experimental males had great difficulty defending their territo-
ries as compared with controls. When experimental birds tried to de-
fend their territories, intruding males remained for long periods and
seemed to ignore the experimental male, even when he apparently went
through all the usual maneuvers of territorial defense. In one study
(Smith, 1972), experimental males that maintained their territories had
no obvious problem attracting females (although harem sizes of exper-
imentals and controls were not compared); in the other study, exper-
imental males attracted females only after the black paint covering their
epaulets was chipped away. There are two possible explanations for
the inability of experimental males to defend their territories: (1) they
may have been mistaken for Euphagus blackbirds (Brewer's or Rusty)
that are all-black, or (2) they may have lacked a required sign stimulus
of threat. Hansen and Rohwer (1986) compared these two hypotheses
and found that Red-winged Blackbird males were able to discriminate
between mounted Brewer's Blackbirds and epaulet-blackened Red-
winged Blackbirds. Noting that intruding Red-winged Blackbirds cover
their epaulets, Hansen and Rowher concluded that experimental birds
were mistaken for intruders, i.e., they lacked the sign stimulus of threat
normally displayed by owners.
Burley et a1. (1982; see also Harvey, 1986, and references cited
therein) found that both sexes of zebra finches preferred particular
colors of plastic leg bands. Ratcliffe and Boag (1987) showed that the
colors of leg bands did not affect male-male interactions and that female
preferences for male leg bands were not expressed when male-male
interactions were an important determinant of mating success.
Another study has contrasted the importance of epigamic versus
agonistic sexual selection, in this case not for colorfulness, but rather
for a conspicuous morphological feature. Andersson (1982b) showed
that female Long-tailed Widowbirds (Euplectes progne) mate prefer-
entially with males that have experimentally lengthened tails as com-
pared with males with norlIlal or experimentally shortened tails. An-
dersson was able to demonstrate that the improved mating success of
the long-tailed males was not attributable to increased success in
male-male competition.
A mostly observational study suggests that the colorful plumage
of adult male manakins functions in male-male competition and not
in female choice (Foster, 1987). Foster found that males in subadult
plumages successfully copulated with females when adult males were
absent, either naturally (rare) or when experimentally removed. She
also found that adult males were more aggressive to other adult males
than they were to subadult males. Thus, the subadult plumage lowered
male aggression, but not at the expense of attractiveness to females.
Under normal circumstances, male dominance relationships ensured
that subadult males did not copulate with females.
Houde (1987) found in guppies that male-male competition did
not occur over mates; thus, the brightly colored spots of male guppies
are favored only because of female preference (Houde, 1987, and ref-
erences cited therein).
We know of no other studies that were able to separate out epigamic
from agonistic sexual selection. Most studies have considered either
one or the other. We consider agonistic sexual selection first, then
epigamic.
6.5.1. Agonistic Sexual Selection

The strongest evidence to date that coloration has a threat function
comes from the nonbreeding season. When female Chaffinches (Frin-
gilla coelebs) were dyed to resemble males, the experimental birds rose
in status against both males and females, even though most males re-
lIlained dominant to the dyed females (Marler, 1955). Similarly, when
immature White-crowned Sparrows (Zonotrichia 1eucophrys) (Parsons
and Baptista, 1980; Fugle et a1., 1984) and Harris' Sparrows (Zonotri-
chia queru1a) (Rohwer, 1985) were dyed to resemble adults, they rose
in status relative to other immature birds of their species. Thus, the
signal normally correlated with sex (in Chaffinches) or age (in White-
crowned and Harris' Sparrows), hence with dominance status, was
respected independently of any other cues of status or fighting ability.
There is a lot of evidence that coloration acts as a releaser of aggres-
sion during the breeding season (Lack, 1939; Peiponen, 1960, in Eibl-
Eibesfeldt, 1970; D. Smith in the television movie, "Why Birds Sing");
however, coloration cannot be favored because it acts as a releaser of
aggression unless for some peculiar reason the colorful individual ben-
efits by being attacked (Rowland, 1982). The studies of color as a releaser
of aggression usually involve presenting a relevant patch of color to a
defending individual. If these results can be taken as evidence that
coloration has a threat function during the breeding season, it is because
we predict that if the same patch of coloration were presented to an
intruding individual, the intruder would be deterred. Recently, R0skaft
and Rohwer (1987) tested this prediction using male Red-winged Black-
bird dummies: they found that male Red-wings landed closer to dum-
mies with normal red epaulets than to dummies with enlarged red
epaulets and that male Red-wings landed closer to dummies with black-
ened epaulets than to an empty pole. When the four treatments were
presented at once, male Red-wings were more likely to land near a
dummy with blackened epaulets or an empty pole than they were to
land near either mount with epaulets. Thus, the red epaulet acts as a
deterrent to male Red-wings, whereas the black body coloration appears
to attract male Red-wings (R0skaft and Rohwer, 1987).
Evidence that coloration is important for territorial defense comes
from a number of species in which males and females defend separate
territories during part of the year and in which both sexes are colorful,
i.e., Great Tit (Lack, 1966; Fretwell, 1972), European Robin (Erithocus
rubeculo) (Lack, 1965), Red-headed Woodpecker (Melonerpes erythro-
cepholus) (Kilham, 1978), and three species of hummingbirds (Wolf,
1969, 1975; Bleiweiss, 1985). The woodpecker and the hummingbirds
are especially noteworthy because most species in their families are
sexually color dimorphic.
Lorenz (1962, 1966) found a correlation between colorfulness and
territoriality in a Caribbean community of coral reef fish. By contrast,
Ehrlich et 01. (1977) found that most species of colorful butterfly fish
(Chaetodontidae) on the Great Barrier Reef of Australia were neither
territorial nor aggressive. In addition, a literature search by Ehrlich et
01. (1977) demonstrated many species of coral reef fish (especially in
Pomacentridae) that were territorial but cryptic in coloration. Both Pe-
terman (1971) and Brown et 01. (1973) found associations between so-
ciality and coloration, but they were not the ones predicted by agonistic-
signaling hypotheses. Peterman found that all schooling, rock-dwelling,

and coral-dwelling fishes in the Bahamas are colorful, whereas seven
of nine substrate-dwelling fishes are not. The schooling fishes are es-
sentially nonaggressive, despite being colorful. In Kenya, all eight social
species studied were colorful and essentially nonaggressive (Brown et
01., 1973).
6.5.2. Epigamic Sexual Selection

Most of the studies of female preferences for particular color pat-
terns have occurred in polymorphic species (many of these studies were
considered in Section 5), but in addition there are at least three ex-
perimental studies and one correlative study. Two of the experimental
studies were discussed above (Andersson, 1982b; Burley, 1986). The
other experimental study, involving an aviary population of weaver-
birds, demonstrated that the lack of a particular color pattern lowered
the mating success of males (Collias et 01., 1979): young females more
than older females refused to lay eggs with males that had their normally
yellow underwings dyed black. The young females often formed tem-
porary pair bonds with the dyed males, but deserted them before laying
eggs.
Hamilton and Zuk (1982) argued that brightly colored feathers should
show the effects of ectoparasites or general poor health due to disease
more readily than do duller colors. Thus, they argued that females
should choose brightly colored males that appear healthy and free of
ectoparasites. In support of their hypothesis, they found a weak but
significant correlation between bright male coloration and parasite load
in North American passerines. Read (1987) extended their study by
adding European passerines and by testing for a number of confounding
factors and reconfirmed the correlation.
6.6. Mate Choice or Mate Attraction

If a signal to potential conspecific mates, is colorfulness an object
of mate choice or an object for mate attraction? The epigamic portion
of nonrandom mating in birds can be divided into mate attraction, mate
choice, mate seeking, or forced copulation. Mate seeking and forced
copulation are both consistent with cryptic coloration, but either mate
attraction or mate choice might favor conspicuous coloration in the
attractive or chosen mate. Both mate attraction and mate choice might
operate simultaneously in a single species, so the presence of each
needs to be assessed independently.
Mate choice (sometimes referred to as "active mate choice") im-

plies, empirically, that in searching for a quality breeding situation,
females discriminate between conspecific males. As a consequence of
acquiring information and of rejecting some males, females pay at least
some small time or energetic cost for their behavior. To justify paying
this cost, females must derive some tangible benefit, which may be
environmental (Le., nonheritable characteristics such as a good nesting
territory) or genetic (Le., "good genes" that would be preferred by all
females or complementary genes that some females would choose and
others reject). A number of hypotheses, many of which are controver-
sial, have been proposed to explain the benefits that females receive
from choosing mates. These are considered in Section 6.6.1. A recent
laboratory experiment on the red flour beetle (Tribolium castaneum)
tested for a correlation between attractiveness and heritable differences
in the viability of offspring but found none (Boake, 1986). A number
of studies with the same aim will be required to evaluate whether this
process occurs in nature.
Mate attraction usually involves situations in which males arrive
on a breeding territory or an advertising site (such as a lek) and advertise
for mates. Males differ in mating success, but only because they are
differentially successful in attracting females, not because of female
choice. Thus, females do not reject males or otherwise incur costs of
mate choice, and differential male mating success can occur even if
there is no benefit to female choosiness. Other investigators have used
such terms as "mate choice," "mate preference," or "passive mate choice"
for this phenomenon; however, because differential mate attraction has
no cost or benefit to the female, these terms are paradoxical and con-
fusing. Female attraction might occur to a nonadaptive (= selectively
neutral) trait of males (Lande, 1981; Kirkpatrick, 1982, 1987) or to a
trait that renders males more conspicuous (Parker, 1982, 1983). These
possibilities are considered in Section 6.6.2.
In deciding whether either mate choice or mate attraction might
favor colorfulness in birds, it is necessary to perform a color manipu-
lation by obscuring any color pattern believed to be the object of epi-
gamic selection. If obscuring the color pattern lowers the mating success
of experimental individuals, a close look at the results should enable
a determination as to whether the color pattern was an object of choice
or attraction. Choice implies that at least some females visit and reject
some males. The number of males visited by females should be ob-
servable in a number of field and laboratory situations (Janetos, 1980;
Thornhill, 1980; Brown, 1981). If the color pattern is used as an object
of mate choice, then visitation rates of females to experimental males
should remain high, but their mating success should be low. If con-
spicuousness were the important quality of the color patch, then a
manipulation that dramatically lowers conspicuousness should have a
greater effect on mating success of experimentals than an equally dra-
matic manipulation that has less effect on conspicuousness. If females
prefer a color patch for arbitrary reasons, then the experimental males
with that patch obscured should show low mating success, but the
system should include little "shopping" behavior among females.
These predictions are essentially untested. Butcher (1984) found
extensive "shopping" behavior in female "Bullock's" Orioles (Icterus
galbula bullockii), but they did not discriminate against males whose
black plumage had been bleached to a dull orange. The results suggest
that there is mate choice in female "Bullock's" Orioles, but that the
choice is not for black male coloration or for the black-orange color
contrast. Unfortunately, the manipulation did not significantly lower
the conspicuousness of the male orioles, nor were sample sizes suffi-
cient to detect a subtle change in the experimental males' acceptability
to females.
Houde (1987) suggested that mate choice was more important than
mate attraction in female preferences for conspicuous male guppies
because she could demonstrate no difference in the distance of attrac-
tion of females to males that differed in conspicuousness and because
females did differ in their sexual responsiveness and in their willing-
ness to copulate with males that differed in conspicuousness.
6.6.1. Mate Choice

If females choose mates based on their coloration, what evolu-
tionary benefit might they derive? Females who nest on a male's ter-
ritory should choose males with good territories, and females whose
mates feed them or their young should choose males that are good
foragers; these conclusions are not controversial. However, in these
species, females should be able to assess territory quality and foraging
ability directly, and they should not rely on male coloration as indi-
cators.
Females might also choose males on the basis of genetic comple-
mentarity. There should be an optimal level of inbreedingloutbreeding
(Bateson, 1983); in addition, there might be particular loci at which
homozygosity or heterozygosity is favored. A color patch might be an
indication of genotype in either of these cases, allowing assortative or
disassortative mating (see Section 5).
Far more controversial is the idea that a female might pick a mate
for his "good genes." The idea is that the male's good genes should be
correlated with higher survival and reproductive success of his off-
spring. A number of investigators reject the idea of mate choice for
improved offspring survival because they believe that there is little
additive genetic variance for traits that are closely tied to fitness (Ar-
nold, 1983, and references cited therein). However, even if there is a
small amoung of variance, mate choice will be favored (Maynard Smith,
1985); thus, a low rate of occurrence of slightly deleterious mutations
seems sufficient to account for mate choice for improved offspring sur-
vival (Kondrashov, 1984; Manning, 1984). Some data are beginning to
accumulate about additive genetic variance for fitness in natural pop-
ulations; to date, the data are inconclusive Oones, 1987). Partridge (1980)
showed in Drosophila melanogaster that the offspring of females given
a choice of mates were more successful than the offspring of females
who were forced to copulate with a single male. Similar results are
found in plants with and without a choice of pollen (Stephenson and
Bertin, 1983).
Even if there is additive genetic variance for survival or competitive
ability, why should conspicuousness be positively correlated with such
genes? Conspicuous coloration is energetically cheap and easy to mimic;
thus, it should not provide good information concerning genetic quality.
In addition, conspicuous coloration exposes its bearer to predators and
rivals, which should lower the survival of conspicuous individuals
relative to cryptic ones. There are at least three ways in which coloration
might facilitate mate choice within species: (1) by serving as a handicap,
(2) by advertising a display, or (3) by advertising the health of the
plumage. These are considered in the next three paragraphs.
To argue that conspicuous coloration indicates survival or com-
petitive ability is to argue that the individual has been able to survive
or be present on territory despite the handicap of being conspicuous
(Zahavi, 1981; Borgia, 1979). Thus, a conspicuous bird that is alive and
available as a potential mate is more likely to be of high genetic quality
than a similar cryptic individual because it has been subjected to a
higher probability of detection by predators (the handicap principle:
Zahavi, 1975, 1977; Kodric-Brown, 1985) or competitors (Borgia, 1979).
Models of this hypothesis require that (1) only individuals of high
quality acquire conspicuous coloration (phenotypic plasticity), (2) fe-
males choose the best among the colorful individuals, or (3) the benefit
of being preferred as a mate (the Fisher effect) is included (Andersson,
1982a; Dominey, 1983; Kodric-Brown and Brown, 1984; Nur and Has-
son, 1984; Maynard Smith, 1985; Andersson, 1986).
A male might demonstrate his health and agility in an energetically
costly or difficult-to-perform display; conspicuous coloration may be

selected to accentuate this display. In this case, the display provides
the information about health and agility and the coloration advertises
the display.
Finally, brightly colored feathers may show the effects of ectopar-
asites or general poor health due to disease more readily than do duller
colors (Hamilton and Zuk, 1982). Females would prefer brightly colored
males because they can be more sure that they are free of ectoparasites
or other disease.
To date, the theories in this area are way ahead of the data. Direct
tests of these three ideas may be difficult to devise, but acceptance of
them will require confirmation of unique predictions in field and lab-
oratory studies.
6.6.2. Mate Attraction

If females are passively attracted to males on the basis of their
coloration, are they attracted to conspicuous males, or are they at-
tracted to males with an arbitrary patch of color? One of the most
nonintuitive results (for biologists trained in the adaptationist school)
of recent theoretical models of sexual selection has been the finding by
Lande (1981) and Kirkpatrick (1982) that females might mate prefer-
entially with males with certain characteristics even if those charac-
teristics decreased male survival and even if the females derived no
benefit at all from mating with those males.
There are two keys to making the model work: (1) females suffer
no cost from their preference for these males, and (2) the increase in
mating success of these preferred males must be greater than the loss
in survival or fecundity caused by the characteristic that also causes
the female preference. The result is nonintuitive for two reasons: (1)
the models appear to be about female preference, but female preference
has no cost or benefit, and (2) it does not seem logical that a trait that
lowers male survival should be favored by sexual selection.
Because the models involve no costs or benefits for female pref-
erences, selection acts on the male trait alone. Thus, we prefer to con-
sider these as models of the mate attracting behavior of males. This
change in focus makes the results seem more reasonable.
In reference to the second point, it is exactly this idea of a trade-
off between reproduction and survival that has become a central tenet
of life-history theory (Williams, 1966; Stearns, 1976). In life-history
theory, the amount of effort expended on current reproduction is lim-
ited primarily by the effect of such efforts on survival, hence on future
reproduction. Mate attraction is vital for successful reproduction, thus

any trait that improves an individual's success in attracting a mate will
be favored as long as the resulting increase in reproductive success
outweighs any resulting loss in survival probability or fecundity (Kirk,
patrick, 1982). This is so because fitness is a multiplicative function of
survival success times mating success times fecundity.
Parker (1982, 1983) has also modeled the mate-attracting behavior
of males under the assumption that there is no cost or benefit to females;
however, his models add one critical element missing in the Lande and
Kirkpatrick models. Parker argues that males are competing to increase
their radius of attraction to increase the chance that they will be heard
or seen by receptive females. Thus, the key element of Parker's models
is that mate attraction selects for conspicuous male traits, not just ar-
bitrary male traits.
Parker's model makes two predictions not made by the Lande and
Kirkpatrick models: (1) that exaggerated coloration should always be
in the direction of increasing conspicuousness, and (2) that a color
manipulation that affects conspicuousness should affect mating success
more severely than an equally drastic color manipulation that does not
affect conspicuousness.
6.7. Agonistic Presence or Quality

If an agonistic signal to conspecifics during the breeding season,
does coloration signal presence (the priority hypothesis) or quality (the
fighting-ability hypothesis)? Priority effect is one of a number of names
for the observation that individuals in a number of species often win
contests because they have priority over their opponents with respect
to a particular resource, such as a territory or a mate (Maynard Smith,
1982, and references cited therein). The priority effect consists of two
distinct but interrelated phenomena: (1) challenger defeat (i.e., defend-
ers defeat challengers in escalated contests), and (2) challenger inhi-
bition (i.e., challengers retreat from defenders without fully escalating).
Challenger defeat may occur for one of two categories of reasons
(Maynard Smith, 1982, and references cited therein): (1) defenders are
on average better fighters than challengers, either because defenders
are individuals that are able to pursue the resource earlier or because
a high frequency of fights early in the period of resource possession
results in only the best fighters being defenders, or (2) resources are
more valuable to defenders than to challengers because (a) defenders
know how to optimize energy gain on the territory (Davies and Houston,
1981), (b) defenders have stable relationships with their neighbors (Krebs,
1982), or (c) defenders know less than challengers about the options
available to challengers (Rohwer, 1982).
Challenger inhibition may occur (1) because defenders would be
expected to win an escalation for either of the two above reasons, (2)
because fights are so risky that a challenger would be better off to forego
a challenge even if he could win (Rohwer, 1982; Maynard Smith, 1982),
(3) because there are good alternatives to fighting defenders, or (4)
because of an "arbitrary" asymmetry "defender wins" that is uncor-
related with fighting ability or resource value (Maynard Smith, 1982).
Good alternatives to fighting defenders occur when there is excess suit-
able habitat (resulting in the ideal free distribution of Fretwell, 1972),
or when defenders frequently abandon resources (for reasons other than
losing fights; e.g., Davies, 1978). The priority effect may be reinforced
when information about relative fighting ability or differential valuation
of resources is not available because of typical intensity displays or
plumage monomorphism. When fighting is risky (point 2) but the al-
ternatives are poor (the opposite of point 3), a "war of attrition" may
be initiated by the challenger rather than escalation or abandonment
of the resource to the defender.
The threat hypothesis assumes that coloration improves the success
of colorful individuals in agonistic interactions. Coloration is advan-
tageous for defenders when it improves challenger defeat or challenger
inhibition. Threat coloration must work in one of three ways: by low-
ering the rate of agonistic encounters of colorful individuals, by causing
an encounter to be shorter or less escalated, or by improving the like-
lihood that colorful individuals will win an escalated fight. Unlike
antlers or other morphological features, coloration cannot directly im-
prove its bearer's fighting ability; therefore, coloration is unlikely to
improve challenger defeat; rather, it must aid in challenger inhibition.
Coloration may act as a distance signal of threat (favoring con-
spicuousness) or as a sign stimulus of threat (favoring distinctiveness).
If conspicuousness is most important, threat coloration should operate
by lowering the number of encounters with competitors. If distinctive-
ness is most important, threat coloration should operate by reducing
repeat encounters, by shortening the length of encounters or by low-
ering the probability that a competitor will escalate against a colorful
individual.
Why should coloration improve challenger inhibition? The present
authors split on this issue: one of us (Rohwer, 1982) supports the fight-
ing-ability hypothesis (F AH), whereas Butcher favors a priority hy-
othesis (PH) (as outlined later in this section).
By the F AH, colorfulness is favored in good fighters when distinc-
tive coloration renders fight winners more memorable, lessening the

likelihood that challengers will repeat a fight with a distinctive winner.
The FAH should apply best to species in which fighting is risky; in
these species, challengers should collect information about a large num-
ber of defenders (to determine the worst fighter) and fight only rarely
(to avoid the risks). As the colorful badge of fighting ability spreads,
challengers might avoid fights with all badge bearers after one defeat
with a badge bearer. As a result, all defenders in a species may become
colorful because poor fighters mimic good fighters to avoid being sin-
gled out by challengers. As a result, defenders should be conspicuous
and largely monomorphic. However, exceptionally good fighters are
selected to diverge from the appearance of the mimics to restore the
benefits of an honest badge of fighting ability. Therefore, different pop-
ulations (species) should be very different in plumage because new
patches (of arbitrary color and location) are constantly being favored
in good fighters of a population and mimicked by poor fighters of that
population. This process could be responsible for the "leapfrog" pattern
of color differences among subspecies in the Andes Mountains of South
America (Remsen, 1984) and for the very different appearance of many
pairs of hybridizing species.
By contrast, the PH argues that colorfulness is favored in any in-
dividual that benefits from the priority effect, regardless of relative
fighting ability. Thus, colorfulness, within the context of defense of
resources, is a badge of priority that works whenever the priority effect
works. Colorfulness serves as either a distance signal or as a sign stim-
ulus of threat.
The two hypotheses make a number of exclusive predictions. The
FAH predicts that a color badge should be most likely to evolve when
challenger inhibition and challenger defeat are not complete (because
some defenders are better able to defeat challengers than others). Ac-
cording to the FAH, defenders should be cryptic if challenger inhibition
is complete because priority should be the asymmetry used to decide
the contest, not coloration. By contrast, the PH asserts that color is the
badge of priority and should be most beneficial when challenger in-
hibition is most complete and there are few escalations. The FAH pre-
dicts that if an artificial color badge is added to a defender that is a
good fighter, he should face fewer challengers (especially fewer repeat
visits from challengers); if a badge is added to a defender that is a poor
fighter, he should face more challengers (more repeat visits). The PH
predicts that in both cases, the number of challengers should stay the
same or decline, since they are both defenders and both should benefit
from advertising their priority. If intrusion ratef! were to rise in both

groups, a species recognition function is suggested.
7. CONCLUSIONS
The study of bird coloration is exciting because the theories of bird

coloration derive from such a number of different fields in biology. This
review would have been much different without recent advances in
our understanding of thermal physiology, aggression, sexual selection,
and communication. Research on bird coloration has the potential to
contribute to each of these fields.
On the other hand, the large number of potential explanations for
color patterns has probably inhibited progress because of the inherent
difficulty in addressing a large number of hypotheses simultaneously.
Most studies of bird coloration to date have advocated a single hy-
pothesis, without seriously testing that hypothesis against alternatives.
However, the review dispelled any notions we may have had that a
single hypothesis might account for a wide variety of color patterns by
accounting for the costs and benefits of conspicuous coloration under
various circumstances. We hope we have suggested a number of ap-
proaches to testing a large number of the available hypotheses. We argue
that conspicuousness or distinctiveness are the essential qualities for
signals, despite the difficulty of quantifying these qualities in nature.
We present three major empirical rules of avian color dimorphism:
When there are differences, males are more colorful than females, adults
are more colorful than young birds, and breeding-season birds are more
colorful than non breeding-season birds. These patterns indicate that
some form of sexual selection must be an important selective factor
favoring colorfulness. Thus, we spend much of the review covering a
variety of sexual selection hypotheses in detail. The three rules are also
consistent with the threat hypothesis; that coloration helps individuals
defend resources during the breeding and nonbreeding seasons. The
threat hypothesis may also help explain monomorphic species and
species with plumage variability within sex and age classes.
A large number of species feature color dimorphisms or polymor-
phisms that are independent of sex, age, and season. These species
provide many of the best animals for studying the variety of selective
pressures of plumage coloration; these studies confirm that a wide va-
riety of selective pressures are important.
A lot of evidence suggests that black and white provide physio-
logical benefits to their bearers. However, few studies have compared

black and white birds with similar cryptically colored individuals. Thus,
the interrealtionship between physiological colors and signaling colors
is still poorly understood.
A recent monograph (Baker and Parker, 1979) was dedicated to the
idea that most conspicuous coloration functions to signal predators that
the colorful individuals are unprofitable prey. Most of their arguments
support the idea that conspicuous birds are less vulnerable to predation
than are cryptic birds, but this correlation is consistent with the sexual
selection hypotheses. To date there have been no tests of the two central
ideas of the unprofitable-prey hypothesis: (1) that predators choose not
to pursue conspicuous prey, and (2) that conspicuous prey are more
difficult to catch than cryptic prey. Paying attention to the context of
colorful displays should help determine whether colorfulness is aimed
at conspecifics, predators, or prey.
Very few species of birds molt twice a year. Thus, plumage worn
during one season may be primarily an adaptation to another season.
If sexual selection is the major force favoring colorfulness and predation
is the major force favoring crypsis, older birds of species that are colorful
year-round may be too colorful in the nonbreeding season for maximal
survival, and younger birds that are relatively cryptic year-round may
be too cryptic in the breeding season for maximal breeding success.
Conspicuous coloration has traditionally been considered as an
isolating mechanism, preventing interspecific hybridization. However,
little evidence and little theory exist to support this idea. Rather, species
isolation appears to be an unselected by-product of color differences
that arise during allopatry.
Both agonistic and epigamic sexual selection seem to favor col-
orfulness in some species. A few field and laboratory studies have been
able to separate out the two, but in many species, both will prove
important. Both forms of sexual selection for conspicuous coloration
provide strong theoretical challenges in explaining precisely why col-
orfulness is favored.
There are three major epigamic sexual selection arguments, al-
though much of the recent discussion has focused on just two. Color-
fulness might help females choose males with "good genes" for a variety
of reasons, or females might choose males with an arbitrary color badge
despite detrimental effects on offspring survival. The third alternative
is that males might compete among themselves to be more conspicuous
to females, with females mating more frequently with the more con-
spicuous males. Theoretical models exist for all three possibilities, but
very few data are available from the field or laboratory to determine
whether any of these mechanisms are likely to be important in nature.

We expect that a number of these studies are probably already under-
way, and developments in this area should be dramatic during the next
few years.
We have initiated a debate about how colorfulness might aid re-
source defenders within relatively monomorphic classes of individuals.
Rohwer favors the fighting-ability hypothesis, which states that good
fighters benefit by having a unique badge of fighting ability, but poor
fighters benefit by mimicking good fighters. Butcher favors the priority
hypothesis, which states that all individuals that can win contests just
because of their priority over the contested resource should advertise
their priority through conspicuous coloration.
Our review of the status of research on bird coloration confirms
that a number of fascinating questions remain. Are conspicuous birds
signaling to predators? Are some classes of birds stuck in a suboptimal
plumage for half the year because of the cost of molt? Does conspicuous
male coloration help females choose "good genes" for survival? Are
there delicately balanced opposing selective pressures that can account
for the maintenance of plumage polymorphisms or dimorphisms that
are unrelated to age or sex? We hope that the next few years will produce
answers to these and other questions that will dramatically increase
our understanding of the importance of conspicuous plumage colora-
tion-and extravagant morphological structures-in the lives of birds.
ACKNOWLEDGMENTS. Gordon Orians has provided helpful comments

on a number of drafts of this manuscript. George Williams, Michael
Beecher, and Allen Rutberg provided detailed and helpful comments
on an early version; William Langbauer critiqued a more recent version.
Malte Anderson, Mercedes Foster, Torbjorn Jarvi and Morten Bakken,
Anders Moller, Geoffrey Parker, Trevor Price, and William Searcy pro-
vided unpublished manuscripts. We thank all these individuals for
their help.
REFERENCES
A. O. U., 1983. Check-Jist of North Americon Birds. 6th ed .. American Ornithologists'
Union. Washington. D.C.
Andersson. M .. 1982a. Sexual selection. natural selection. and quality advertisement.
BioI. J. Linn. Soc. 17:375-393.
Andersson. M .. 1982b. Female choice selects for extreme tail length in a widowbird.
Noture (Lond.) 299:818-820.
Andersson, M., 1983, On the functions of conspicuous seasonal plumages in birds, Anim.
Behav.31:1262-1264.
Andersson, M., 1986, Evolution of condition-dependent sex ornaments and mating pref-
erences: Sexual selection based on viability differences, Evolution 40:804-816.
Arnold, S. J., 1983, Sexual selection: The interface of theory and empiricism, in: Mate
Choice (P. Bateson, d.), pp. 67-107, Cambridge University Press, Cambridge.
Arnold, S. J., and Wade M. J., 1984, On the measurement of natural and sexual selection:
Applications, Evolution 38:720-734.
Bailey, S. F., 1978, Latitudinal gradients in colors and patterns of passerine birds, Condor
80:372-381.
Baker, R R, 1985, Bird coloration: In defence of unprofitable prey, Anim. Behav. 33:
1387-1388.
Baker, R R., and Hounsome, M. V., 1983, Bird coloration: Unprofitable prey model
supported by ringing data, Anim. Behav. 31:614-615.
Baker, R E., and Parker, G. A., 1979, The evolution of bird coloration, Philos. Trans. R.
Soc. Lond. 8287:63-130.
Balph, M. H., Balph, D. F., and Romesburg, H. C., 1979, Social status signaling in winter
flocking birds: An examination of a current hypothesis, Auk 96:78-93.
Bateson, P., 1983, Optimal outbreeding, in: Mate Choice (P. Bateson, ed.), Cambridge
University Press, Cambridge, pp. 257-277.
Beehler, B., 1983, Frugivory and polygamy in birds of paradise, Auk 100:1-12.
Beehler, B., and Pruett-Jones, S. G., 1983, Display dispersion and diet of birds of paradise:
A comparison of nine species, Behav. Ecol. Sociobiol. 13:229-238.
Bischoff, R J., Gould, J. L., and Rubenstein, D. 1., 1985, Tail size and female choice in
the guppy (Poecilia reticulata), Behav. Ecol. Sociobiol. 17:253-256.
Bleiweiss, R, 1985, Iridescent polychromatism in a female hummingbird: Is it related to
feeding strategies?, Auk 102:701-713.
Boake, C. R B., 1986, A method for testing adaptive hypotheses of mate choice, Am.
Nat. 127:645-666.
Borgia, G., 1979, Sexual selection and the evolution of mating systems, in: Sexual Se-
lection and Reproductiv8 Competition in Insects (M. S. Blum and N. A. Blum, eds.),
Academic, New York, pp. 19-80.
Borowski, R, 1982, Tailspots of Xiphophorus and the evolution of conspicuous poly-
morphism, Evolution 35:345-358.
Brian, A. D., 1949, Dominance in the Great Tit (Parus major), Scott. Nat. 61:144-155.
Brown, J. H., Cantrell, M. A., and Evans, S. M., 1973, Observations on the behaviour and
coloration of some coral reef fish (Family: Pomacentridae), Mar. Behav. Physiol. 2:
63-71.
Brown, J. L., 1963, Aggressiveness, dominance and social orgainization in the Stellar Jay,
Condor 65:460-484.
Brown, L., 1981, Patterns offemale choice in mottled sculpins (Cottidae, Teleostei), Anim.
Behav. 29:375-382.
Burley, N., 1981, The evolution of sexual indistinguishability, in: Natural Selection and
Social Behavior (R D. Alexander and D. W. Tinker, eds.), Chiron, New York, pp.
121-137.
Burley, N., 1986, Comparisons of the band-colour preferences of two species of estrildid
finches, Anim. Behav. 34:1732-1741.
Burley, N., Krantzberg, G., and Radman, P., 1982, Influence of colour-banding on the
conspecific preferences of zebra finches, Anim. Behav. 30:444-455.
Burtt, E. H., Jr., 1979, Tips on wings and other things, in: The Behavioral Significance
of Color (E. H. Burtt, Jr., ed.), Garland STPM Press, New York and London, pp.
75-110.
Burtt, E. H., Jr., 1981, The adaptiveness of animal colors, Bioscience 31:723-729.
Burtt, E. H., Jr., 1986, An analysis of physical, physiological, and optical aspects of avian
coloration with emphasis on wood-warblers, Ornithol. Monog. [AOUl 38:1-126.
Butcher, G. S., 1984, Sexual color dimorphism in orioles (the Genus Icterus): Tests of
communication hypotheses, unpublished Ph.D. dissertation, University of Wash-
ington, Seattle.
Butlin, R., 1987, Speciation by reinforcement, Trends Ecol. Evol. 2:8-13.
Caldwell, G. S., 1981, Attraction to mixed-species heron flocks, Behav. Ecol. Sociobiol.
8:99-103.
Caldwell, G. S., 1986, Predation as a selective force on foraging herons: Effects of plumage
color and flocking, Auk 103:494-505.
Caro, T. M., 1986, The functions of stotting in Thomson's gazelles: Some tests of the
predictions, Anim. Behav. 34:663-684.
Chen, D.-M., and Goldsmith, T. H., 1986, Four spectral classes of cone in the retinas of
birds, J. Compo Phys. A159:473-479.
Clements, J., 1981, Birds of the World: A Checklist, 3rd ed., Facts on File, New York.
Clutton-Brock, T. H., and Harvey, P. H., 1984, Comparative approaches to investigating
adaptation, in: Behavioural Ecology: An Evolutionary Approach 0. R. Krebs and N.
B. Davies, eds.), 2nd ed., Blackwell Scientific Publications, Oxford, pp. 7-29.
Colgan, P., 1983, Comparative Social Recognition, Wiley, New York.
Collias, E. c., Collias, N. E., Jacobs, c. H., McAlary, F., and Fujimoto, J. T., 1979, Ex-
perimental evidence for facilitation of pair formation by bright color in weaverbirds,
Condor 81:91-93.
Collias, N. E., 1943, Statistical analysis of factors which make for success in initial
encounters between hens, Am. Nat. 77:519-538.
Cooke, F., and Davies, J. c., 1983, Assortative mating, mate choice, and reproductive
fitness in Snow Geese, in: Mate Choice (P. Bateson, ed.), Cambridge University Press,
Cambridge, pp. 279-295.
Cooke, F., Findlay, C. S., Rockwell, R. F., and Smith, J. A., 1985, Life history studies in
the Lesser Snow Goose (Ansel' caerulescens caerulescens). III. The selective value
of plumage polymorphism: new fecundity, Evolution 39:165-177.
Cott, H. B., 1946, The edibility of birds, Proc. Zool. Soc. Lond. 116:371-524.
Cott, H. B., 1985, Palatability of birds and eggs, in: A Dictionary of Birds [B. Campbell
and E. Lack, eds.], Poyser, Calton, p. 427.
Cott, H. B., and Benson, C. W., 1970, The palatability of birds, mainly based upon
observations of a tasting panel in Zambia, Ostrich Suppl. 8:357-384.
Coutlee, E. 1., 1967, Agonistic behavior in the American Goldfinch, Wilson Bull. 79:
89-100.
Cracraft, J., 1981, Toward a phylogenetic classification of the recent birds of the world
(Class Aves), Auk 98:681-714.
Crook, J. H., 1964, The evolution of social organization and visual communication in the
weaverbirds (Ploceinae), Behaviour Suppl. 10:1-178.
Croze, H., 1970, Searching image in Carrion Crows, Z. Tierpsychol. Beiheft 5:1-86.
Curio, E., 1976, The Ethology of Predation, Springer-Verlag, Berlin.
Darwin, c., 1871, The Descent of Man, and Selection in Relation to Sex, John Murray,
London (1890, 2nd ed.)
Davies, N. B., 1978, Territorial defence in the speckled wood butterfly (Pararge aegeria),
the resident always wins, Anim. Behav. 26:138-147.
Davies, N. B., and Houston, A. I., 1981, Owners and satellites: The economics of territory
defense in the Pied Wagtail, Motacilla alba, J. Anim. Ecol. 50:157-180.
Dawkins, R., and Krebs, J. R., 1979, Arms races between and within species, Proc. R.
Soc. Lond. B Biol. Sci. 205:489-504.
Dilger, W. C., 1956, Hostile behavior and reproductive isolating mechanisms in the avian
genera Catharus and Hylocichla, Auk 73:313-353.
Dilger, W. C., 1960, Agonistic and social behavior of captive red polls, Wilson Bull. 72:
114-132.
Dixon, K. 1., 1963, Some aspects of social organization in the Carolina Chickadee, Pro-
ceedings XIII International Ornithological Congress, June 17-24, 1962, C. G. Sibley,
ed., American Ornithologists' Union, Baton Rouge, Louisiana, pp. 240-258.
Dobzhansky, T., 1937, Genetics and the Origin of Species, Columbia University Press,
New York.
Dominey, W. J., 1983, Sexual selection, additive genetic variance and the "phenotypic
handicap," ]. Theor. Bioi. 101:495-502.
Dwight, J., 1900, The sequence of plumages and moults of the passerine birds of New
York, Ann. NY Acad. Sci. 13:73-360 (1975: repr.).
Ehrlich, P. R., Talbot, F. H., Russell, B. C., and Anderson, G. R. V., 1977, The behaviour
of chaetodontid fishes with special reference to Lorenz' "poster coloration" hypoth-
esis, J. Zool. Lond. 183:213-228.
Eibl-Eibesfeldt, 1.,1970, Ethology: The Biology of Behavior, Holt, Rinehart, and Winston,
New York.
Endler, J. A., 1978, A predator's view of animal color patterns, in: Evolutionary Biology,
Vol. 11 (M. K. Hecht, W. C. Steere, and B. Wallace, eds.), Plenum, New York, pp.
319-364.
Endler, J. A., 1980, Natural selection on color patterns in Poecilia reticulata, Evolution
34:76-91.
Endler, J. A., 1983, Natural and sexual selection on color patterns in poeciliid fishes,
Environ. Biol. Fishes 9:173-190.
Endler, J. A., 1987, Predation, light intensity, and courtship behaviour in Poecilia reti-
culata (pisces: Poeciliidae), Anim. Behav. 35:1376-1385.
Ewald, P. W., and Rohwer, S. A., 1980, Age, coloration, and dominance in nonbreeding
hummingbirds: A test of the asymmetry hypothesis, Behav. Ecol. Sociobiol. 7:273-279.
Findlay, C. S., Rockwell, R. F., Smith, J. A., and Cooke, F., 1985, Life history studies of
the Lesser Snow Goose (Anser caerulescens caerulescens). VI. Plumage polymor-
phism, assortative mating, and fitness, Evolution 39:904-914.
Fisher, R. A., 1930, The Genetical Theory of Natural Selection, Clarendon Press, Oxford
(1958, 2nd ed., Dover, New York).
Forbush, E. H., and May, J. B., 1929, Birds of Massachusetts and Other New England
States. III. Land Birds from Sparrows to Thrushes, Norwood Press, Norwood
Massachusetts.
Ford, E. B., 1975, Ecological Genetics, 4th ed., Chapman and Hall, London; Wiley, New
York.
Foster, M. S., 1987, Delayed maturation, neoteny, and social system differences in two
manakins of the genus Chiroxiphia, Evolution 41:547-558.
Fretwell, S. D., 1972, Populations in a Seasonal Environment, Princeton University Press,
Princeton, New Jersey.
Fugle, G. N., Rothstein, S. I., Os enberg, C. W., and McGinley, M. A., 1984, Signals of
status in wintering White-crowned Sparrows, Zonotrichia leucophrys gambelii, Anim.

Behav. 32:86~93.
Gardarsson, A., 1971, Food ecology and spacing behavior of Rock Ptarmigan Lagopus
mutus in Iceland, unpublished Ph.D. dissertation, University of California, Berkeley.
Gilliard, E. T., 1969, Birds of Paradise and Bower Birds, Weidenfeld and Nicolson,
London; Natural History Press, Garden City, New Jersey.
Glase, J., 1973, Ecology of social organization in the Black-capped Chickadee, Living Bird
12:235~267.
Goodwin, D., 1951, Some aspects of the behaviour of the jay Garrulus glandarius, Ibis
93:414~442, 602~625.
Goodwin, D., 1960, Sexual dimorphism in pigeons, Bull. Br. Ornithol. Club 80:45~52.
G6tmark, F., 1987, White underparts in gulls function as hunting camouflage, Anim.
Behav. 35:1786~1792.
Gould, S. J., and Lewontin, R. c., 1979, The spandrels of San Marco and the Panglossian
paradigm: A critique of the adaptationist programme, Proc. R. Soc. Lond. B 205:
581~598.
Grant, P. R., 1965, Plumage and the evolution of birds on islands, Syst. Zool. 14:47~52.
Grant, P. R., 1975, The classic case of character displacement, in: Evolutionary Biology,
Vol. 8 (T. Dobzhansky, M. K. Hecht, and W. C. Steere, eds.), Plenum, New York, pp.
237~337.
Hailman, J. P., 1959, Why is the male Wood Duck strikingly colorful?, Am. Nat. 93:
383~384.
Hailman, J. P., 1960, A field study of the Mockingbird's wing-flashing behavior and its
association with foraging, Wilson Bull. 72:346~357.
Hailman, J. P., 1967, Spectral discrimination: An important correction, J. Opt. Soc. Am.
57:281~282.
Hailman, J. P., 1976, Uses of the comparative study of behavior, in: Evolution, Brain,
and Behavior: Persistent Problems (R. B. Masterton, W. Hodos, and H. Jerison, eds.),
Erlbaum, Hillside, New Jersey, pp. 13~22.
Hailman, J. P., 1977, Optical Signals: Animal Communication and Light, Indiana Uni-
versity Press, Bloomington.
Hailman, J. P., 1979, Environmental light and conspicuous colors, in: The Behavioral
Significance of Color (E. H. Burtt, Jr., ed.), Garland STPM Press, New York, pp.
289~354.
Hall, B. P., Moreau, R. E., and Galbraith, I. C. J., 1966, Polymorphism and parallelism in
the African bush-shrikes of the genus Malaconotus (including Chlorophoneus), Ibis
108:161~182.
Hamilton, T. H., 1961, On the functions and causes of sexual dimorphism in breeding
plumage of North American species of warblers and orioles, Am. Nat. 95:121~123.
Hamilton, T. H., and Barth, R. H., Jr., 1962, The biological significance of seasonal change
in male plumage appearance in some New World migratory species, Am. Nat. 96:
129~144.
Hamilton, W. D., and Zuk, M., 1982, Heritable true fitness and bright birds: A role for
parasites?, Science 218:384~387.
Hamilton, W. J. III, 1973, Life's Color Code, McGraw-Hill, New York.
Hamilton, W. J. III, and Peterman, R. M., 1971, Counters hading in the colourful reef fish
Chaetodon lunula: Concealment, communication, or both?, Anim. Behav. 19:357~364.
Hansen, A. J., and Rohwer, S., 1986, Coverable badges and resource defence in birds,
Anim. Behav. 34:69~76.
Hardy, J. W., 1967, Evolutionary and ecological relationships between three species of
blackbirds (Icteridae) in central Mexico, Evolution 21:196-197.
Hardy, J. W., and Dickerman, R. W., 1965, Relationships between two forms of Red-
winged Blackbirds in Mexico, Living Bird 4:107-130.
Harvey, P. H., 1986, Birds, bands, and better broods?, Trends Ecol. Evol. 1:8-9.
Harvey, P. H., and Greenwood, P. H., 1978, Anti-predator defence strategies: Some ev-
olutionary problems, in: Behavioural Ecology: An Evolutionary Approach (J. R. Krebs
and N. B. Davies, eds.), Blackwell Scientific Publications, Oxford, pp. 129-15l.
Hilborn, R., and Stearns, S. C., 1982, On inference in ecology and evolutionary biology:
The problem of multiple causes, Acta Biotheor. 31:145-164.
Hill, G. E., 1988, The function of delayed plumage maturation in male Black-headed
Grosbeaks, Auk 105:1-10.
Hinde, R. A., 1956, A comparative study of the courtship of certain finches (Fringillidae),
Ibis 98:1-23.
Hingston, R. W. G., 1933, The Meaning of Animal Colour and Adornment, E. Arnold,
London.
Holyoak, D. T., 1973, Significance of colour dimorphism in Polynesian populations of
Egretta sacra, Ibis 115:419-420.
Houde, A. E., 1987, Mate choice based on naturally occurring color-pattern variation in
a guppy population, Evolution 41:1-10.
Huxley, J. S., 1938, Threat and warning coloration in birds, with a general discussion of
the biological functions of color, in: Proceedings of the Eighth International Orni-
thological Congress, F. C. R. Jourdain, ed., The University Press, Oxford, pp. 430-455.
Huxley, J. S., 1955, Morphism in birds, Acta Int. Ornithol. Congr. XI, July 1934, A.
Portman and E. Sutter, eds., Birkhauser Verlag, Basel and Stuttgart, Switzerland, pp.
309-328.
Immelman, K., 1972, The influence of early experience upon the development of social
behaviour in estrildine finches in: Proceedings of the XV International Ornithological
Congress August 30-September 5, 1970, (K. H. Voous, ed.), E. J. Bull, Leiden, Neth-
erlands, pp. 316-338.
Immelman, K., 1975, The evolutionary significance of early experience, in: Function and
Evolution in Behaviour (G. Baerends, C. Beer, and A. Manning, eds.), Clarendon,
Oxford, pp. 243-253.
Jackson, W. M., Rohwer, S., and Winnegrad, R. L., 1988, Status signaling is absent within
age-and-sex classes of Harris' Sparrows, Auk 105:424-427.
Janetos, A. C., 1980, Strategies of female choice: A theoretical analysis. Behav. Ecol.
Jarvi, T., and Bakken, M., 1984, The function of the variation in the breast stripe of the
great tit, Anim. Behav. 32:590-596.
Johnson, N. K., and Brush, A. H., 1972, Analysis of polymorphism in the Sooty-capped
Bush Tanager, Syst. Zool. 21:245-262.
Jones, J. S., 1985, The heritability of fitness: Bad news for good genes?, Trends Ecol. Evol.
2:35-38.
Kear, J., 1970, The adaptive radiation of parental care in waterfowl, in: Social Behaviour
in Birds and Mammals: Essays on the Social Ethology of Animals and Man (J. H.
Crook, ed.), Academic, London, pp. 357-39l.
Ketterson, E. D., 1979, Aggressive behavior in wintering dark-eyed juncos: Determinants
of dominance and their possible relation to geographic variation in the sex ratio,
Wilson Bull. 91:371-383.
Kikkawa, j., 1961, Social behavior of the white-eye Zosterops latera lis in winter Hocks,
Ibis 103:428-442.
Kilham, 1., 1974, Early breeding season behavior of Downy Woodpeckers, Wilson Bull.
86:407-418.
Kilham, 1., 1978, Sexual similarity of Red-headed Woodpeckers and possible explana-
tions based on fall territorial behavior, Wilson Bull. 90:285-287.
Kiltie, R. A., 1988, Countershading: Universally deceptive or deceptively universal'!,
Trends Ecol. Evol. 3:21-24.
King. j. R., 1980, Energetics of avain moult, in: Acta XVII Congr. Internatl. Ornithol., R.
Niihring, ed., Verlag der Deutschen Ornithologen Gesellschaft, Berlin, pp. 312-317.
Kirkpatrick, M., 1982, Sexual selection and the evolution of female choice, Evolution 36:
1-12.
Kirkpatrick, M., 1987, Sexual selection by female choice in polygynous animals, Annu.
Rev. Ecol. Syst. 18:43-70.
Knapton, R. W., and Krebs, j. R., 1976, Dominance hierarchies in winter Song Sparrows,
Condor 78:567-569.
Kodric-Brown, A., 1985, Female preference and sexual selection for male coloration in
the guppy (Poecilia reticulata), Behav. Ecol. Sociobiol. 17:199-206.
Kodric-Brown, A., and Brown j. H., 1984, Truth in advertising: The kinds of traits favored
by sexual selection, Am. Nat. 124:309-323.
Kondrashov, A. S., 1984, Deleterious mutations as an evolutionary factor.!. The advantage
of recombination, Genet. Res. 44:199-217.
Krebs, j. R., 1979, Bird colours, Nature (Lond.) 282:14-16.
Krebs, j. R., 1982, Territorial defence in the Great Tit (Parus major): Do residents always
win?, Behav. Ecol. Sociobiol. 11:185-194.
Kushlan, j. A., 1977, The significance of plumage colour in the formation of feeding
aggregations of ciconiiforms, Ibis 119:361-364.
Lack, D., 1939, The behaviour of the robin. I, II. Proc. Zool. Soc. Lond. A 109:169-178.
Lack, D., 1954, The Natural Regulation of Animal Numbers, Clarendon. Oxford.
Lack, D., 1965, The Life of the Robin, Collins, London.
Lack, D., 1966, Population Studies of Birds, Clarendon, Oxford.
Lack, D., 1968, Ecological Adaptations for Breeding in Birds, Methuen, London.
Lack, D., 1970, The endemic ducks of remote islands, Wildfowl 5:5-10.
Lande, R., 1981, Models of speciation by sexual selection on polygenic traits, Proc. Nat!.
Acad. Sci. USA 78:3721-3725.
LeCroy, M., 1981, The genus Paradisaea display and evolution, Am. Mus. Nov. 2714:
1-52.
Lewis, D. M., 1972, Importance of face-mask in sexual recognition and territorial behavior
in the yellowthroat, Jack-Pine Warbler 50:98-109.
Loehle, c., 1987, Hypothesis testing in ecology: Psychological aspects and the importance
of theory maturation, Q. Rev. BioI. 62:397-409.
Lorenz, K., 1962, The function of colour in coral reef fishes, Proc. R. Inst. Gr. Br. 39:
282-296.
Lorenz, K., 1966, On Aggression, Harcourt, Brace, and World, New York.
Lowther, J. K., 1961, Polymorphism in the White-throated Sparrow, Zonotrichia albicollis
(Gmelin), Can. J. Zool. 39:281-292.
Lyon, B. E., and Motgomerie, R. D., 1985, Conspicuous plumage of birds: Sexual selec.tion
or unprofitable prey? Anim. Behav. 33:1038-1040.
Lyon, B. E., and Motgomerie, RD., 1986, Delayed plumage maturation in passerine birds:
Reliable signaling by subordinate males?, Evolution 40:604-615.
Lythgoe, J. N., 1979, The Ecology of Vision, Oxford University Press, New York.
Manning, J. T., 1984, Males and the advantage of sex, J. Theor. BioI. 108:215-220.
Marler, P., 1955, Studies of fighting in chaffinches. 2. The effect on dominance relations
of disguising females as males, Br. J. Anim. Behav. 3:137-146.
Martin, S. G., 1970, The agonistic behavior of Varied Thrush (Ixoreus noevius) in winter
assemblages, Condor 72:452-459.
Maynard Smith, J., 1982, Evolution and the Theory of Games, Cambridge University
Press, Cambridge.
Maynard Smith, J., 1985, Sexual selection, handicaps, and true fitness, J. Theor. BioI.
115:1-8.
Mayr, E., 1942, Systematics and the Origin of Species, Columbia University Press, New
York.
Mayr, E., 1965, Animal Species and Evolution, Belknap Press-Harvard University Press,
Cambridge, Massachusetts.
Mayr, E., 1972, Sexual selection and natural selection, in: Sexual Selection and the
Descent of Man 1871-1971 (8. Campbell, ed.), Aldine, Chicago, pp. 87-104.
McKaye, K. R, Kocher, T., Reinthal, P., Harrison, R, and Kornfield, 1., 1984, Genetic
evidence for allopatric and sympatric differentiation among color morphs of a Lake
Malawi cichlid fish, Evolution 38:215-219.
Mock, D. W., 1981, White-dark polymorphism in herons, in: Proceedings of the First
Welder Wildlife Symposium, pp. 145-161.
Monroe, B. 1., Jr., 1964, Wing-flashing in the red-backed scrub-robin, Erythropygia zam-
besiana, Auk 81:91-92.
Montgomerie, R D., and B. E. Lyon, 1986, Does longevity influence the evolution of
delayed plumage maturation in passerine birds?, Am. Nat. 128:930-936.
Moodie, G. E. E., 1972, Predation, natural selection, and adaptation in an unusual Three-
spined Stickleback, Heredity 28:155-167.
Moreau, R E., 1960, Conspectus and classification of the Ploceine weaverbirds, Ibis 102:
298-321.
Moreau, R E., 1966, The Bird Faunas of Africa and Its Islands, Academic, London.
Morony, J. J., Bock, W. J., and Farrand, J., 1975, Reference List of Birds of the World,
Department of Ornithology, American Museum of Natural History, New York.
Morton, E. S., 1976, The adaptive significance of dull coloration in yellow warblers,
Condor 78:423.
Moynihan, M., 1960, Some adaptations which help to promote gregariousness, in: Pro-
ceedings of the XII International Ornithological Congress, June 5-12, 1958, G. Berg-
man, K. O. Donner, and 1. von Haartman, eds., Tilgmann Kirjapaino, Helsinki, Fin-
land, pp. 523-541.
Murton, R K. and Westwood, N. J., 1977, Avian Breeding Cycles, Clarendon Press,
Oxford.
Murton, R K., Westwood, N. J., and Thearle, R J. P., 1973, Polymorphism and the
evolution of a continuous breeding season in the pigeon, Columbia livia, J. Reprod.
Fertil. Suppl. 19:563-577.
Nur, N., and Hasson, 0., 1984, Phenotypic plasticity and the handicap principle, J. Theor.
BioI. 110:275-297.
Oberholser, H. C., 1974, Bird Life of Texas, University of Texas Press, Austin, Texas.
O'Donald, P., 1959, Possibility of assortative mating in the Arctic Skua, Nature (Lond.)
183:1210.
O'Donald, P., 1980, Genetic Models of Sexual Selection, Cambridge University Press,
Cambridge, Massachusetts.
O'Donald, P., Davis, J. W. F., and Broad, R. A., 1974, Variation in assortative mating in
two colonies of Arctic Skuas, Nature (Land.) 252:700-701.
Odum, E. P., 1942, Annual cycle of the Black-capped Chickadee. 3, Auk 59:499-531.
Olson, S. 1., 1982, A critique of Cracraft's classification of birds, Auk 99:733-739.
Orians, G. H., and Christman, G. M., 1968, A comparative study of the behavior of Red-
winged, Tricolored, and Yellow-headed Blackbirds. Univ. Calif. Pub1. Zoo1. 84:1-81.
Parker, G. A., 1982, Phenotype-limited evolutionarily stable strategies, in: Current Prob-
lems in Sociobiology (King's College Sociobiology Group, eds.), Cambridge Univer-
sity Press, Cambridge, pp. 173-201.
Parker, G. A., 1983, Mate quality and mating decisions, in: Mate Choice (P. Bateson, ed.),
Cambridge University Press, Cambridge, pp. 141-166.
Parrish, J. W., Ptacek, J. A., and Will, K. 1., 1984, The detection of near-ultraviolet light
by nonmigratory and migratory birds, Auk 101:53-58.
Parsons, J., and Baptista, L. F. 1980, Crown color and dominance in the White-crowned
Sparrow, Auk 97:807-815.
Partridge, 1., 1980, Mate choice increases a component of offspring fitness in fruit flies,
Nature (Lond.) 283:290-291.
Paulson, D. R., 1973, Predator polymorphism and apostatic selection, Evolution 27:269-277.
Payne, R. B., 1967, Interspecific communication signals in parasitic birds, Am. Nat. 101:
363-375.
Payne, R. B., 1982, Ecological consequences of song matching: Breeding success and
intraspecific song mimicry in Indigo Buntings, Ecology 63:401-411.
Peek, F. W., 1972, An experimental study of the territorial function of vocal and visual
display in the male Red-winged Blackbird (Agelaius phoeniceus), Anim. Behav. 20:
112-118.
Peiponen, V. A., 1960, Verhaltensstudien am blaukehlchen, Ornis Fenn. 37:69-83.
Peterman, R. M., 1971, A possible function of coloration in coral reef fishes, Copeia 1971:
330-331.
Peterson, R. T., 1980, A Field Guide to the Birds, Houghton-Mifflin, Boston.
Pierotti, R., 1987, Isolating mechanisms in seabirds, Evolution 41:559-570.
Platt, J. R., 1964, Strong inference, Science 146:347-353.
Price, T. D., 1984, Sexual selection on body size, territory and plumage variables in a
population of Darwin's finches, Evolution 38:327-341.
Ratcliffe, 1. M., and Boag, P. T., 1987, Effects of colour bands on male competition and
sexual attractiveness in zebra finches (Poephila guttata), Can. ,. Zool. 65:333-336.
Read, A. F., 1987, Comparative evidence supports the Hamilton and Zuk hypothesis on
parasites and sexual selection, Nature (Lond.) 328:68-70.
Remington, C. 1., 1968, Suture-zones of hybrid interaction between recently joined biotas,
Evol. BioI. 2:321-428.
Remsen, J. V., Jr., 1984, High incidence of "leapfrog" pattern of geographic variation in
Andean birds: Implication for the speciation process, Science 224:171-173.
Ricklefs, R. E., and Cox, G. W., 1972, Taxon cycles in the West Indian avifauna, Am.
Nat. 106:195-219.
Ridley, M., 1983, The Explanation of Organic Diversity, Oxford University Press, Oxford.
Rockwell, R. F., Findlay, C. S., Cooke, F., and Smith, J. A., 1985, Life history studies of
the Lesser Snow Goose (Anser caerulescens caerulescens). IV. The selective value
of plumage polymorphism: Net viability, the timing of maturation, and breeding
propensity, Evolution 39:178-189.
Rohwer, S., 1975, The social significance of avian winter plumage variability, Evolution
29:593-610.
Rohwer, S., 1982, The evolution of reliable and unreliable badges of fighting ability, Am.
Zool. 22:531-546.
Rohwer, S., 1983, Formalizing the avoidance-image hypothesis: Critique of an earlier
prediction, Auk 100:971-974.
Rohwer, S., 1985, Dyed birds achieve higher social status than controls in Harris' spar-
rows, Anim. Behav. 34:1325-1331.
Rohwer, S., 1986~A previously unknown plumage of first-year Indigo Buntings and
theories of delayed plumage maturation, Auk 103:281-292.
Rohwer, S., and Butcher, G. S., 1988, Winter versus summer explanations of delayed
plumage maturation in temperate passerine birds, Am. Nat. 131:556-572.
Rohwer, S., and Ewald, P. W., 1981, The cost of dominance and advantage of subordi-
nation in a badge signaling system, Evolution 35:441-454.
Rohwer, S., and Niles, D. M., 1979, The subadult plumage of male Purple Martins:
Variability, female mimicry, and recent evolution, Z. Tierpsychol. 51:282-300.
Rohwer, S., and Paulson, D. R, 1987, The avoidance-image hypothesis and color poly-
morphism in Buteo hawks, Ornis Scand. 18:285-290.
Rohwer, S., Fretwell, S. D., and Niles, D. M., 1980, Delayed maturation in passerine
plumages and the deceptive aquisition of resources, Am. Nat. 115:400-437.
Rohwer, S., Ewald, P. W., and Rohwer, F. C., 1981, Variation in size, appearance, and
dominance within and among the sex and age classes of Harris' Sparrows, J. Field
Ornithol. 52:291-303.
Rohwer, S., Klein, W. P. Jr., and Heard, S., 1983, Delayed plumage maturation and the
presumed prealternate molt in American Redstarts, Wilson Bull. 95:199-208.
Roskaft, E., and Jarvi, T., 1983, Male plumage colour and mate choice of female Pied
Flycatchers Ficedula hypoleuca, Ibis 125:396-400.
Roskaft, E., and Rohwer, S., 1987, An experimental study of the function of the epaulettes
and the black body colour of male red-winged blackbirds, Anim. Behav. 35:1070-1077.
Roskaft, E., Jarvi, T., Nyholm, N. E. I., Virolainen, M., Winkel, W., and Zang, H., 1986,
Geographic variation in secondary sexual plumage colour characteristics of the male
Pied Flycatcher, Ornis Scand. 17:293-298.
Rowland, W. J., 1982, The effects of male nuptial coloration on stickleback aggression:
A reexamination, Behaviour 80:118-126.
Samson, F. B., 1977, Social dominance in winter flocks of Cassin's Finch, Wilson Bull.
89:57-66.
Schutz, F., 1965, Sexuelle pragung bei Anatiden, Z. Tierpsychol. 22:50-103.
Selander, R K., 1965, On mating systems and sexual selection, Am. Nat. 99:129-141.
Selander, R. K., 1972, Sexual selection and dimorphism in birds, in: Sexual Selection
and the Descent of Man 1871-1971 (B. Campbell, ed.), Aldine, Chicago, pp. 180-230.
Selander, R. K., and Hunter, D. K., 1960, On the function of wing-flashing in mockingbirds,
Semler, D. E., 1971, Some aspects of adaptation in a polymorphism for breeding colours
in the Threespine Stickleback (Gasterosteus aculeatus), J. Zool. 165:291-302.
Shield, W. M., 1977, The social significance of avian winter plumage variability: A
comment, Evolution 31:905-906.
Sibley, C. G., 1957, The evolutionary and taxonomic significance of sexual dimorphism
and hybridization in birds, Condor 59:166-191.
Sibley, C. G., and Ahlquist, J. E., 1983, Phylogeny and classificaion of birds based on the
data of DNA-DNA hybridization, Current Ornithol. 1:245-292.
Skutch, A. F., 1940, Some aspects of Central American bird-life, Sci. Mthly. 51:409-418,
500-511.
Skutch, A. F., 1957, The resident wood warblers of Central America, in: The Warblers
of America (1. Griscom and A. Sprunt, eds.), Devin-Adair, New York. pp. 275-285.
Smith, D. G., 1972, The role of the epaulets in the Red-winged Blackbird (Agelaius
phoeniceus) social system, Behaviour 41:251-268.
Smith, N. G., 1966, Evolution of some arctic gulls (Larus): An experimental study of
isolating mechanisms, Ornith. Monogr. (AOU) 4:1-99.
Smith, S. M., 1980, Henpecked males: The general pattern in monogamy?, J. Field Or-
nithol. 51:55-64.
Stearns, S. c., 1976, Life-history tactics: A review of the ideas, Q. Rev. BioI. 51:3-47.
Stephenson, A. G., and Bertin, R. I., 1983, Male competition, female choice, and sexual
selection in plants, in: Pollination Biology (1. Real, ed.), Academic. New York, pp.
109-149.
Studd, M. V., and Robertson, R. J., 1985, Life span, competition, and delayed plumage
maturation in male passerines: The breeding threshold hypothesis, Am. Nat. 126:
101-115.
Thompson, W. 1., 1960, Agonistic behavior in the House Finch. II. Factors in aggres-
siveness and sociality, Condor 62:378-402.
Thorneycroft, H. G., 1975, A cytogenetic study of the White-throated Sparrow, Zonotri-
chia albicollis, Evolution 29:611-621.
Thornhill, R, 1980, Mate choice in Hylobittacus apical is (Insecta: Mecoptera) and its
relation to some models of female choice, Evolution 34:519-538.
Tordoff, H. B., 1954, Social organization and behavior in a flock of captive, nonbreeding
Red Crossbills, Condor 56:346-358.
Trivers, R. 1., 1972, Parental investment and sexual selection, in: Sexual Selection and
the Descent of Man 1871-1971 (B. Campbell, ed.)., Aldine, Chicago, pp. 136-179.
Verner, J., and Willson, M. F., 1969, Mating systems, sexual dimorphism, and the role
of North American passerine birds in the nesting cycle, Omithol. Monogr. (AOU) 9:
1-76.
Wallace, A. R., 1889, Darwinism: An Exposition of the Theory of Natural Selection with
Some of Its Applications, Macmillan, London.
Walsberg, G. E., 1982, Coat color, solar heat gain, and conspicuousness in the Phaino-
pepla, Auk 99:495-502.
Walsberg, G. E., 1983, Ecological energetics: What are the questions?, in: Perspectives in
Ornithology (A. H. Brush and G. A. Clark, eds.), Cambridge University Press, Cam-
bridge, pp. 135-158.
Walsberg, G. E., Campbell, G. S., and King, J. R., 1978, Animal coat color and radiative
heat gain: Are-evaluation, J. Compo Phys. 126:211-222.
Watson, G. E., 1962, Sympatry in palearctic Alectoris partridges, Evolution 16:11-19.
Watt, D. J., 1986a, A comparative study of status signalling in sparrows (genus Zonotri-
chia), Anim. Behav. 34:1-15.
Watt, D. J., 1986b, Relationship of plumage variability, size and sex to social dominance
in Harris' sparrows, Anim. Behav. 34:16-27.
Watt, D. J., Ralph, C. J., Atkinson, C. T., 1984, The role of plumage polymorphism in
dominance relationships of the White-throated Sparrow, Auk 101:110-120.
Weldon, P. J., and Burghardt, G. M., 1984, Deception divergence and sexual selection,
Z. Tierpsychol. 65:89-102.
West-Eberhard, M. J., 1983, Sexual selection, social competition, and speciation, Q. Rev.
BioI. 58:155-183.
Whitfield, D. P., 1986, Plumage variability and territoriality in breeding turnstone Ar-
enaria interpres: Status signalling or individual recognition?, Anim. Behav. 34:
1471-1482.
Whitfield, D. P., 1987, Plumage variability, status signalling and individual recognition
in avian flocks, Trends Ecol. Evol. 2:13-18.
Williams, E. E., and Rand, A. S., 1977, Species recognition, dewlap function, and faunal
size, Am. Zool. 17:265-274.
Williams, G. C., 1966, Adaptation and Natural Selection. A Critique of Some Current
Evolutionary Thought, Princeton University Press, Princeton, New Jersey.
Willis, E. 0., 1972, The behavior of spotted antbirds, Ornithol. Monogr. (AOU) 10:1-162.
Witherby, H. F., Jourdain, F. C. R., Ticehurst, N. F., and Tucker, B. W., 1943, The Hand-
book of British Birds, Vol. I, Crows to Firecrest, Witherby, London.
Wolf, 1. 1., 1969, Female territoriality in a tropical hummingbird, Auk 86:490-504.
Wolf, 1. 1., 1975, Female territoriality in the Purple-throated Carib, Auk 92:511-522.
Wunderle, J. M., Jr., 1981, An analysis of a morph ratio cline in the Bananaquit (Coereba
flaveola) on Grenada, West Indies, Evolution 35:333-344.
Wunderle, J. M., Jr., 1983, A shift in the morph ratio cline in the Bananaquit of Grenada,
West Indies, Condor 85:365-367.
Zahavi, A., 975, Mate selection-A selection for a handicap, ,. Theor. BioI. 53:205-214.
Zahavi, A., 1977, The cost of honesty, J. Theor. BioI. 67:603-605.
Zahavi, A., 1981, Natural selection, sexual selection, and the selection of signals, in:
Evolution Today (G. G. E. Scudder and J. L. Reveal, eds.), Proceedings of the Second
International Congress on Systematic and Evolutionary Biology, July 17-24, 1980,
Hunt Institute for Botanical Documentation, Carnegie-Mellon University, Pittsburg,
Pennsylvania, pp. 133-138.
Zumpe, D., 1965, Laboratory observations on the aggressive behaviour of some butterfly
fishes, Z. Tierpsychol. 22:226-236.
CHAPTER 3
ATMOSPHERIC STRUCTURE AND

AVIAN MIGRATION
PAUL KERLINGER and FRANK R. MOORE
1. INTRODUCTION
Why do some birds migrate during daytime and others at night? Why
do some fly at high altitudes and others at lower altitudes'? Whereas
no comprehensive explanation of the diel schedule and altitude of
migration has been proposed, several hypotheses have been advanced
to explain nocturnal migration. These hypotheses focus on the need to
forage during daylight (Brewster, 1886; Palmgren, 1949; Dorst, 1962),
on predator avoidance (Lincoln, 1952), and on avoidance of atmo-
spheric turbulence (Nisbet, 1955; Raynor, 1956; Bellrose, 1967). In ad-
dition, some authorities have suggested that the daily timing of migra-
tion is related to dietary habits or mode of migratory flight (Dorst, 1962;
Baker, 1978). We argue that the diel schedule and altitude of bird mi-
gration have evolved in response to predictable variations in the struc-
ture of the atmosphere during its daily cycle.
To test the hypothesis that atmospheric structure is an important
selective force in the evolution of the diel incidence and altitude of
migration, we first examine atmospheric phenomena that are relevant
to migratory flight. From our analysis of atmospheric structure, we make
predictions regarding the optimal diel timing and altitude of migration.
PAUL KERLINGER • Cape May Bird Observatory, Cape May Point, New Jersey
08212. FRANK R. MOORE • Department of Biological Sciences, University of South-
ern Mississippi, Hattiesburg, Mississippi 39406-5018.
l(Hl
110 PAUL KERLINGER and FRANK R. MOORE
We then test our predictions by reviewing the literature concerned with

diel timing and altitude of migrants. After testing the predictions, we
examine the merit of alternate explanations of the diel timing of mi-
gration in the light of data supporting the atmospheric structure hy-
pothesis. The rationale for examining altitude of flight in the same
framework as diel timing of migration is that atmospheric structure
covaries with time of day and altitude above the ground.
2. ATMOSPHERIC STRUCTURE
The atmosphere through which migrants fly is variable; it is a well-

structured and reasonably predictable medium. A diel pattern of hor-
izontal and vertical movement, as well as temperature and humidity
fluctuations, prevails over much of the world's surface. Some of these
properties are common knowledge, although few reviews in either the
meteorological or ornithological literature detail the properties of that
region of the atmosphere in which most bird migration occurs. It is
surprising that so few avian biologists have considered the importance
of atmospheric structure, although Griffin (1969) recognized that "the
ecology of the atmosphere through which birds travel is an important
though neglected aspect of migration."
The portion of the atmosphere that is important to migrants oc-
cupies the first 2000 + m aboveground level. Vertical and horizontal
movements of air within this layer are called microscale or local phe-
nomena (Oke, 1978; Stull, 1986) to distinguish them from larger phe-
nomena such as high- and low-pressure cells. To understand how these
properties influence migratory flight, we reviewed literature from the
atmospheric sciences concerning vertical and horizontal motion, as
well as temperature and humidity. Because the literature does not pro-
vide all the information needed, we analyzed Local Climatological Data
Monthly Summaries for surface conditions and Summaries of Constant
Pressure Data (WBAN-33 report forms) for conditions up to 700 mbar
(mbar = millibars of mercury, in this case about 3000 m; National Cli-
matological Center, Asheville, North Carolina). Data were from Albany,
New York (42 42' N, 73 40' W; elev. 84 m) and Lake Charles, Loui-
0 0
siana (30 0 07' N, 93 0 13'W; elev. 3 m). These locations were chosen
because both have been the sites of intensive migration research and
because atmospheric structure at these locations should be similar to
that in many temperate and subtropical locations where a preponder-
ance of migratory activity occurs. The periods 1 April-15 May and 16
September-30 October 1984 for Lake Charles and 16 April-30 May and
ATMOSPHERIC STRUCTURE AND MIGRATION 111
1 September-15 October 1984 for Albany were defined operationally

as the migration seasons for atmospheric analyses. The convective depth
was determined from sounding and surface information according the
method described by Cipriano and Kerlinger (1985) and the World
Meteorological Organization (1978).
2.1. Vertical Wind

Vertical motion of the atmosphere, often referred to as thermal
convection, is a form of turbulence that occurs as solar heating warms
the earth's surface (Oke, 1978). It is not strictly vertical because changes
of wind direction and speed distort the true vertical flow of air. If air
above the ground is cooler than the surface air, and becomes cooler
with altitude at a rate faster than the lapse rate (superadiabatic cooling),
the atmosphere becomes unstable. Temperature and pressure gradients
cause warm air to rise until it loses heat or reaches warmer air and
becomes stable. Temperature inversions, with warm air above cooler
surface air, prevent the formation of thermal convection and the at-
mosphere remains stable. Topographical discontinuities such as hills,
as well as differences in absorbance (albedo) and reflectance (emissiv-
ity) of the surface influence the rate and strength of convective devel-
opment (Oke, 1978).
Thermal convection begins shortly after sunrise and dissipates late
in the day before or near sunset (Fig. 1). The rate of vertical development
of the convective layer in early-midmorning is linear (Konrad, 1970;
Rowland, 1973; Kerlinger and Gauthreaux, 1985a), beginning about 1
to 2 hr after dawn and continuing past midday. The rate of ascent of
the convective layer depends on cloud cover, topography, and season
of year. Rates of vertical growth average between 2 and 8 miles per
minute (120-480 mph). Maximum vertical development of the con-
vective layer occurs between 1100 and 1500 hr ranging to >2000 m
aboveground.
The thermal cell or element is believed to be the ultimate form of
convection in the atmosphere (Woodward, 1949; Oke, 1978) and con-
tributes to much of what is referred to as turbulence. Thermal cells
vary in size, shape, and the way air moves within and around them.
The most common type of convective cell is the type I thermal (Hardy
and Ottersten, 1969), which includes thermals that are capped and
uncapped with cumulus cloud. Less common convective cells include
dust devils, thunderstorms, and organized thermals such as those de-
scribed by Hardy and Ottersten (1969). The latter have various struc-
tures. Some are structured like honeycomb with individual cells rang-
1400
1200 Lake Char I es. LA
3 1000
800
600
.J2
400
200
oL-______ ~ ________ ~ __ . 0___
~
6 9 12 15 18
1400
1200 Albany. NY
3 1000
800
FIGURE 1. Development of thermal
600 fields during spring (filled symbols)
400 and autumn (open symbols) migra-
200 tion seasons. Each point represents
a mean ± SD for the 45-day periods
o as outlined in the text. Thermal field
7 10 13 16 19 depth was determined according to
Time of Day Cipriano and Kerlinger (1985).
ing from 5 to 10 km in diameter and up to about 2 km in height. Each

cell is composed of type I thermal units. Linear arrays of thermals occur
when thermals are aligned forming what is called "thermal streets" by
sailplane pilots. Linear arrays can be several hundred kilometers in
length. The largest and most powerful type of thermal convective struc-
ture is the thunderstorm, which can be tens of kilometers in diameter
and >15 km in height.
Type I thermal cells originate at or slightly above ground level.
Although they are columnar for much of their life (Hardy and Katz,
1969; Wilde et 01., 1985), they eventually leave the surface and move
with the wind. They are then considered "free" or isolated thermals.
Early in the day, these cells are scarce and small, possibly <10 m in
diameter and tens of meters in height. By mid-morning, thermals grow
to several hundred meters in diameter and height (Lenschow, 1970;
Warner, 1970; Konrad and Brennan, 1971). Vertical extent may be as
great as 1000 m, and the thermal may resemble a column (Cipriano,
1975; Hardy and Ottersten, 1969; Konrad, 1970; Konrad and Brennan,
1971). The large variability of the size of thermals and height to which
convective cells rise reflects several factors, including time of day, amount
Lake Charles. LA
1200
1000
§
~t-~'!~!'!'I/I'I~t'l
800
cu
..,
-0
:J 600
;:; 400
<C
200
0
1 234 5 6 7 8 9 10 11 12
Albany. NY
1400
1200
§ 1000
OJ 800
..,
-0
:J
600
;:;
!~~ ~
:;;: 400
FIGURE 2. Monthly mean midday 200
(1200 hr) thermal depths as deter-
mined in Fig. 1. Each data point is 0
a mean ± SD for one month. (Sam- 1 2 3 4 5 6 7 8 9 10 11 12
pIe sizes. N = 28-31 days). Month of Year
of solar input (cloud cover), composition of the earth's surface, topog-

raphy, and horizontal wind. In general, thermal convection is inhibited
in winter at temperate latitudes because of shorter periods of solar input
as well as snow cover and moist surfaces. Thermal activity over water
is rare, occurring only with specific environmental circumstances
(Woodcock, 1975).
Maximum thermal convection, as measured by the mean height to
which thermals rise, occurs in April and May at temperate latitudes,
with a lesser second possible peak in September and October (Fig. 2).
This pattern also reflects the frequency of thermal occurrence. In winter,
thermal convection is often absent for many days and when it occurs
it is not very strong. Hence, cumulus clouds tend to be absent at north-
ern temperate latitudes during this season. In May and June, thermals
are often very strong and abundant. This time of year is preferred by
many sailplane pilots because of the prevalence of fine thermal con-
ditions.
The pattern of airflow within a thermal has been likened to a vortex
ring (Woodward, 1949; Cone, 1962). At the center or core of large ther-
-0
OJ 15
OJ
CL~
(f) (f)
0...
-0
C ""
~
3 OJ
U
4- 0
o 4-
L
OJ ::J
U (f)
C
OJ E FIGURE 3. Wind gradients at Lake
L 0
OJ
4-
L
LL
Charles, LA (circles) and Albany,
4-
o
New York (squares). Each data point
represents the mean difference from
o 1000 2000 3000 surface wind ± SD for 45 days of
Al tJ tude (M) spring migration.
mals, air rises at >3 miles per second (mps). Farther from the thermal
core, vertical currents are 1-3 mps, whereas at the periphery air often
flows downward. Small thermals have maximum vertical updrafts of
<2-3 mps at their cores (Manton, 1977; Pennycuick, 1983). At the
bottom of a thermal air is entrained constantly, as is evident near a
tornado or thunderstorm, so that airflow near a thermal is not the same
as ambient wind. As air rises within a thermal, it mixes with cooler air
and is eventually forced outward when it reaches an inversion layer,
resulting in horizontal air currents.
Before leaving vertical air currents something should be said about
internal gravity waves (sometimes called buoyancy waves). Mentioned
as a factor in the ornithological literature first by Griffin (1969), gravity
waves are nearly ubiquitous in the stably stratified planetary boundary
layer (see Hooke and Jones, 1986). Analogous to ocean waves, these
transverse waves have periods measured in minutes, have amplitudes
as great as 300-500 dynes/cm 2 , and often travel at speeds roughly equal
to the flight speeds of birds (see Balachandran and Done, 1964). Mi-
grants could, in principle, make use of these waves (see Griffin, 1969).
2.2. Horizontal Wind

Both speed and direction of horizontal wind vary with time of day
and altitude. A gradient of horizontal wind velocity is evident from the
surface up to several thousand meters (Fig. 3). Winds at 950 mbar
('"'-'500 m) average >4 mps faster than those at the surface. In central
New York, the gradient is continuous, although in Louisiana the wind
speed does not increase above 950 mbar. It is likely that nocturnal jets,
which are fast-moving laminar sheets of air (Stull, 1986), occur fre-
quently in Louisiana such that winds between 1000 and 950 mbar are
actually moving faster than at higher altitudes. In spring in the southern
T
T
T
T I
0 eo I
?
II ~ l
Ll 1
~
o
"D
C
5 '"
;c 15 :8 ".
L J
E
o
L
4-
OJ 5
U
C
OJ
AI bony. NY
L
OJ
4-
FIGURE 4. Diel fluctuations of wind c~
speed during spring (filled symbols)

n
j
and autumn (open symbols) migra-
tion seasons. A mean difference (from
midnight) ± SO is plotted for differ-
ent times of the day (Ns = 45 days).
o oc j j
Differences in time of day (abscissa) L~~~_ ~_~ _~_~_ ~_.
between locations reflect Greenwich 7 10 II lG 19 22

time. TlmQ of Duy
United States, nocturnal jets might permit more rapid migratory jour-
neys.
Friction from vegetation, buildings, and hills slows the flow of
wind near the surface, creating turbulence and eddies. When horizontal
wind is strong, mechanical updrafts from deflected wind form along
ridges, tree rows, mountains, and other discontinuities. Wind speed
increases with height more rapidly over open terrain, such as water
and prairies than over forests, or irregular terrain.
The strength of horizontal winds also changes with time of day.
Winds close to the surface at midday are stronger than at night or in
early morning (Fig. 4). On average, there is a difference of 2 mps be-
tween wind speed at midday and midnight or dawn. The reason for
this difference is that convective activity reaches its maximum near
midday and through the afternoon. Local winds decrease near sunset
and remain calmer until after dawn. Because thermal convection is
mostly absent at night and early in the morning, wind direction varies
less at this time than at midday when massive quantities of air are
sucked into and forced out of thermal elements. Entrainment of air from
the free atmosphere, above the thermal layer, also represents a large
movement of air.
20
10 LA
...,>-. 0 eo
u -10
E
:J
:r: -20
..., OJ
..c
IT) ~ -30
o
c
u OJ -40
,;;: Q:
E -50
o
'-
4-
o 3 6 9 12 15 18 21
OJ
U
C
OJ
20
L
OJ
4- 10
4-
o
-0 -10
E
:J
:r: -20
! -1
OJ
Q:
30
-40
-50
~~~--~--~--~--~~--~--
4 7 10 13 16 19 22
TIme of Day
FIGURE 5. Diel fluctuations of relative humidity during the spring (filled symbols) and
autumn (open symbols) migration seasons. Means ± SD represent the difference between
relative humidity at midnight and various times of the day (N's = 45 days) at the surface.
Differences in time of day (abscissa) between locations reflect Greenwich time.
2.3. Temperature and Relative Humidity Fluctuations

In addition to changes of airflow patterns between night and day,
differences of air temperature and relative humidity are evident. Surface
air temperatures average 5-7 e lower at midnight than at midday at
D
the locations we examined: Louisiana spring mean difference =

6.6 ± O.4 e (SD), autumn mean difference = 5.7° ± 0.5° C; New York
0 D
spring mean difference = 6.9° ± 0.8°e, autumn mean difference =

7.7° ± 0.7°C; sample sizes = 45 days. In addition, relative humidity is
higher at night and early morning than at midday (Fig. 5). This pattern
is the same throughout much of the temperate zone, except in deserts
and prairies, where the differences are greater.
There is also a decrease of temperature with altitude above the
ground (Fig. 6) called the lapse profile (Oke, 1978). The decrease is
often linear with a change of about 6°C per 1000 m. Coincident with
OJ
o
U
o 1000 2000 3000
,-
<+-
CJ
u;
E
:::' 0 .~ Albany. NY
!' ~~!
~;:I_~ "'c!kl~~!tf!
FIGURE 6. Altitudinal profile of
temperature at sunset from the
ground up to 3000 m during spring
(filled symbols) and autumn (open
symbols) migration seasons. Each
point is a mean ± SD of the differ-
ence between the surface and var- o 1000 2000 3000
ious altitudes for 45 days.
this temperature change is a decrease in relative humidity with altitude

(Fig. 7). Inversions (warmer air with increasing height) sometimes occur
in the first few hundred meters above the ground at night and early
morning (Oke, 1978), but temperatures are still lower than during the
daytime.
To summarize, the portion of the atmosphere in which migrants
fly is characterized by diel variations of vertical wind, horizontal wind,
temperature, and relative humidity. Compared with midday, the night
atmosphere is cooler and more humid; horizontal winds are weaker
and more laminar; and vertical motion is usually absent.
3. PREDICTIONS
3.1. Diel Timing

To make predictions as to the behavior of migrants, we must assume
that the flight behavior of migrants has been shaped by natural selection.
We believe it is reasonable that selection has maximized the distance
a bird travels per unit of time and energy expended. Thus, migrants
should fly at times of the day and at heights where travel is least costly,
t)
Lake Char 1es. LA
100
Ill99qf~t
>-
+-'
"0
E 75
::>
:c
>
OJ
50
.;:;
0
OJ
no: 25
o 1000 2000 3000

8
>- Albany. NY
+-'
-D 100
!~~1r1HAHl
E
::>
:c 75
OJ
;: 50
+-'
0
FIGURE 7. Altitudinal profile of rel-
OJ ative humidity associated with al-
no: 25
titude at sunset during spring (filled
symbols) and autumn (open sym-
0 1000 2000 3000 bols) migration seasons. Shown are
AltItude (M) means ± SD for 45-day periods.
most rapid, and safest. On the basis of the changing diel structure of
the atmosphere presented in Sections 2.1-2.3, we predict that birds
that use powered (flapping) flight should initiate migration at sunset
or shortly thereafter and cease flying within 2-3 hr after sunrise. Our
rationale for this prediction is based upon the physiology and aero-
dynamic performance of flying birds.
First, cool humid air promotes convective heat loss by migrants as
opposed to cooling by evaporation (Blem, 1980). Core temperature of
birds using powered flight rises from rv38-39°C when at rest to 41-44°C
(Hart and Roy, 1966; Tucker, 1968a; Torre-Bueno, 1976, 1978). To pre-
vent overheating, birds dissipate heat by convective heat loss from the
skin and evaporation of water from the respiratory tract. Even tropical
species such as the Budgerigar (Melopsittocus undulotus) must resort
to evaporative heat loss during flight in warm air (Tucker, 1968a) and
cease flight in very warm air. An increase of air temperature from 18-20°C
to 36-37°C results in an increase in evaporative heat loss of 32% (15-47%)
in this species. Linear rate of water loss with increasing temperature
has been shown to occur. Water is a limited resource for flying migrants
(Yapp, 1962; Blem, 1980; Dawson, 1982; however see Salt and Zeuthen,
1960), although some is produced as a by-product of fat metabolism.
Biebach et 01. (1986) noted that some passerines migrating over the
Sahara desert land at dawn and seek shade rather than food. Many of
these birds have large fat deposits and could have continued migrating
after sunrise. Flying at night in cool air reduces evaporative water loss,
promoting longer flights. Large powered migrants such as waterfowl
should be particularly susceptible to overheating because their surface
to volume ratio is lower than that of small birds, which makes cooling,
especially by convection, more difficult. Similarly, fat birds should
overheat faster than lean birds because fat acts as insulation.
Second, less energy is required to fly in cool dense air than in warm
air. Equations presented by Pennycuick (1969, 1975) demonstrate that
the power required for flight is negatively related to air density. Large
birds are influenced more because the energy required to fly is pro-
portional to mass to the 1.01-1.17 power (Pennycuick, 1975; Masman
and Klaassen, 1987). Thus, larger birds or birds with large fat deposits
have more to gain by flying at night because the energetic cost of pow-
ered flight at night is less than flying during daytime.
Third, slower wind at night promotes a safer and sometimes less
costly flight than daytime winds. The relative importance of wind to a
migrant's progress and direction is related to the ratio of air speed to
wind speed (Alerstam, 1981). If winds are favorable for migrants, it
would be advantageous to fly with the strongest winds possible, but
perfectly favorable winds are rare. Small, slow birds are influenced
more by wind speed than are larger faster birds because they are less
able to compensate for lateral or opposing winds.
Fourth, wind at night is more laminar than in daytime, thus pro-
moting energetically efficient flight as well as easier orientation and
navigation. During midday, wind speed and direction in both vertical
and horizontal planes changes constantly such that a bird flying through
a thermal field experiences continual changes of wind speed and di-
rection. It should be emphasized that thermal activity in spring and
autumn is greater than at any other time of the year; thus, birds flying
at these times are confronted with powerful turbulence (see Fig. 2).
Maintaining a straight, level course in the preferred direction with these
conditions is difficult and necessitates energetically costly acceleration
and deceleration in addition to climbing and descending. As with wind
speed, birds with a low ratio of air speed to wind speed are more
influenced by turbulence than are faster birds. Using tracking radar,
Griffin (1973) and Able (1974) showed that nocturnal migrants maintain
relatively straight, level tracks.
Rayner (1956) was one of the first to recognize that a migrant flying
through a thermal or turbulent field must readjust its flight surfaces
continually to maintain constant height and direction. Nisbet (1955)
stated that turbulence disoriented migrants and increased the proba-

bility of stalling when tailwind gusts reduced air speed. Later, Tucker
(1974) related turbulence to "profound" increases of energetic cost of
flight. Because wind may be used as a cue for orientation by some birds
(Able, 1980), the relatively laminar flow of wind at night gives more
reliable information regarding direction than winds in daytime. John-
son's (1969) work with insect migration makes it clear that the nocturnal
atmosphere is more conducive for dispersal and migration than the
diurnal atmosphere.
A second prediction from atmospheric structure is that soaring
birds should fly from mid-morning to late afternoon or sunset. We base
this prediction on the different types of flight used by these birds. The
cost of soaring flight is less than one fourth that of powered flight
(Pennycuick, 1975) and is independent of air speed. Therefore, hawks
do not risk overheating during flight at normal daytime temperatures
and can continually correct for changes of vertical and horizontal wind
without wasting energy. Most importantly, these birds extract energy
for flight from the atmosphere by climbing in updrafts generated mostly
by thermal sources and then gliding to the next thermal.
3.2. Altitude
Predictions as to how high migrants should fly are not as easy to
make as the predictions for diel timing of migration. Pennycuick (1969,
1978) predicted that powered migrants should fly as high as available
oxygen allows. He reasoned that the cooler temperatures at high alti-
tudes reduced evaporative water loss and that the lower density of air
promoted faster travel. Although the former reason is correct, the latter
may be offset by the cost of climbing to high altitudes and the increased
cost of generating lift in thin air. By migrating at night instead of day-
time, migrants realize approximately the same difference of temperature
as would be experienced between the surface and 1000 m during day-
time. Considering the faster winds and the lower air temperatures aloft,
there is probably an optimal range of altitudes at which migrants should
fly. We predict that migrants should fly as low as possible to avoid
strong winds, except when winds are favorable, and as high as possible
to realize cooler temperatures. Thus, a trade-off exists between flying
high and low. Migrants would thus have to sample the wind at various
altitudes and to determine where winds were most favorable (Cochran
and Kjos, 1985). The length of a bird's migration might also be a con-
sideration in making predictions as to how high a bird should fly. For
shorter-distance migrants, climbing to high altitudes might be relatively
ATMOSPHERIC STRUCTURE AND MICRA TION 121
more costly than for longer-distance migrants, especially if the longer

flights must be made nonstop.
Soaring birds are constrained by their mode of flight to the turbulent
layer, so we predict that these migrants should fly mostly within the
first 1000 m and constantly change altitude as they climb in thermals
and descend during interthermal glides.
4. FLIGHT BEHAVIOR: TEST OF PREDICTIONS
To test our predictions, we reviewed the avian migration literature

concerned with diel timing and altitude of migration. Because avian
migrants are heterogeneous with respect to taxonomy, size, aerody-
namic performance, and behavior, they have been divided into two
broad categories; those that use soaring flight and those that use pow-
ered flight. Powered migrants are further divided into passerines and
other small birds, shorebirds, and waterfowl.
4.1. Diel Timing of Migration

Most powered migrants fly at night (Appendix I; Fig. 8a). These
migrants include most of the passerines, large proportions of waterfowl
and shorebirds, as well as a variety of other avian groups. Nocturnal
migration of passerines commences about! hr after sunset and variance
around this time is minimal (Drury and Keith, 1962; Gauthreaux, 1971,
1972; Hebrard, 1971; Alerstam, 1976; Richardson, 1978). The activity
of caged passerine migrants is similarly timed (Berthold, 1975). Shore-
birds sometimes initiate flights 2-3 hr before sunset (Appendix I), al-
though most of these birds begin migration at about the same time as
passerines (Richardson, 1979). Waterfowl are even more variable, ini-
tiating flights through the day and night, but migration commences
most often just after sunset.
The peak of migratory activity for nocturnal migrants occurs prior
to 2200 hr and wanes before midnight. Exceptions to this statement are
found, however (e.g., Graber and Hassler, 1962), especially when noc-
turnal migrants must cross water barriers (Gauthreaux, 1972) and des-
erts (Moreau, 1961; but see Biebach et aI., 1986). In these cases, migrants
have little choice but to continue migration until suitable habitat is
found. Nocturnal migration is reduced after 2200 hr, and is virtually
finished by 0000-0200 hr. Early workers believed that nocturnal mi-
grants flew until dawn when they could make a safe landing (Palmgren,
1949; Dorst, 1962). The timing of initiation and duration of nocturnal
122 PAUL KERLlNGER and FRANK R. MOORE
a Waterfowl
- - L--T - - - - - - - - - T - P - L
Soaring Birds
T P L
Shorebirds Shorebirds
--L-- T--P-L
Passerines - Night Passerines - Night
L- - L -- T-P-L
Passerines - Morning
T- P-L
Passerines - Day
-T-P-L- T-L
o 3 6 9 12 15 18 21 24
Time of Day
b Soaring Birds
*--*
Waterfowl
!:J. !:J.
Shorebirds
0-----0 --------
Passerines - Day
+--+ -
Passerines - Night
+ + ----
o tODD 2000 3000 4000

Altitude (M)
FIGURE 8. (a) Schematic diagram of the diel timing of major groups of migrants (drawn
from Appendix I). Each solid line represents the normal time of migration including
takeoff (T), peak migration (P), and landing (L). Dashed lines indicate that data show
variation. The three lines for passerines are for diurnal migrants (day), nocturnal migrants
flying at night (night), and nocturnal migrants flying shortly after dawn (morning). (h)
Schematic diagram of the altitudinal ranges of major groups of migrants (drawn from
Appendix II). Solid lines represent the norm; dashed lines represent exceptional mea-
surements.
migration is correlated with meteorological variables such as precipi-

tation and wind (reviewed by Richardson, 1978).
Large numbers of passerines that typically migrate at night at times
undertake "morning flights" (Rabol, 1967; Gauthreaux, 1978; Bingman,
1980; Hall and Bell, 1981). These flights commence about 1.5-1 hr after
sunrise and continue for about 2 hr. It is not known whether individual
migrants make 2 hr flights or if these flights are comprised of shorter
flights by larger numbers of migrants. "Morning flight" may function
to compensate for drift incurred by wind during the previous night
(Gauthreaux, 1978) or as onward migration (Bingman, 1980; see also
Moore, 1987).
The migration of passerines that are considered diurnal migrants
commences before sunrise. Radar studies have confirmed that birds
such as Starlings (Sturn us vulgaris) and Chaffinches (FringilJa coelebs)
begin migrating up to 1 hr before sunrise with peak migratory activity
some 2 hr later (0800-0930 hr; Alerstam and Ulfstrand, 1975). Some
of these predawn flights involve larids and other nonpasserines. Diurnal
migration is usually finished by 1100-1200 hr, although some species
such as Wood Pigeons (Columba palumba) continue throughout the
day (Alerstam and Ulfstrand, 1974). Mascher et al. (1962), however,
state that much of the spring migration of this species ends prior to
1000 hr. Many species have a bimodal distribution of diurnal activity
with a second peak after 1500 hr (Alerstam and Ulfstrand, 1975). Thus,
few passerines migrate at midday.
The diurnal flights of many waterfowl species also begin before
sunrise. For example, eiders in Scandinavia begin daily flights during
spring migration at about 0400 hr with the peak occurring before 0800 hr.
These birds also initiate a nocturnal migration at around sunset, ending
before 2100 hr. Thus, two migratory periods exist for this species, but
it is not known whether individual migrants undertake flights at both
times on the same day. This bimodal distribution of migratory activity
probably occurs in other waterfowl as well.
Soaring birds rarely engage in nocturnal migratory flights. These
birds depend on updrafts and initiate migration in mid-morning as
thermals develop. Migration ends when convective activity ceases prior
to, or near sunset. Observers such as Broun (1949), Mueller and Berger
(1973), Smith (1980), and Kerlinger and Gauthreaux (1985a) report peaks
of activity of various species that bracket the period from late morning
to early afternoon. Kerlinger and Gauthreaux (1985a) show that the
timing of takeoff for some hawks is correlated with the onset of thermal
activity. These same migrants did not land until late in the afternoon
(usually after 1600 hr) when thermal activity ceased. Long flights over
water by these birds sometimes continue after sunset, as is the case

with Peregrine Falcons (Falco peregrinus) along the East Coast of the
United States (Cochran, 1985).
4.2. Altitude of Migration

The altitude at which migrants fly varies both within and among
avian groups (Appendix II). One reason for this variation is that mi-
grants must climb, cruise, and descend through several hundred to more
than 2000 m of vertical airspace within one flight. Moreover, migrants
respond to changing weather and topography by climbing or descend-
ing. Superimposed on these variable behavioral patterns are the diffi-
culties encountered when measuring the altitude of migration.
Nocturnally migrating passerines usually fly below 700-800 m above
ground level, although some fly to >3000 m. Radar studies of passerine
migrants flying over land show that 50-90% are below 900 m (Fig. 8b)
(Appendix II). Massive kills at towers are evidence that large numbers
of birds fly below 500 m, at least on nights with reduced visibility
(Brewer and Ellis, 1958; Seets and Bohlen, 1977) and suggest that many
migrants are difficult to detect with radar. Thus, some radar studies
overestimate the altitude of migration.
During flight over water passerines frequently fly at altitudes >1000 m
(Appendix II). Reports by Myres (1964) and Gauthreaux (1972) dem-
onstrate rapid changes of altitude by passerines migrating over the water
at dawn and/or dusk. Passerines migrating over the Gulf of Mexico
during the night ascended from <500 m to >1000 m at dawn. A similar
"dawn ascent" was reported by Myres (1964) for Turdus spp. migrating
over the northeastern Atlantic Ocean from Scandinavia. In contrast to
the dawn ascent over water, "morning flight" over land by passerines
seems to occur below 100 m (Appendix II). The altitude of diurnally
migrating passerines is mostly below 1000 m and some researchers
report flight below 100 m.
On average, shorebirds probably migrate at higher altitudes than
most other birds. Radar studies consistently report altitudes> 1000 m,
but most of these have been of migrants flying over the ocean (Appendix
II). Large numbers of fast, high-flying echoes are not as evident over
land, so high-altitude flight may be related to flight over water, as is
the case with passerines. However, Richardson (1979) found no differ-
ence between the height of shorebirds flying over land and over water.
The birds tracked by Ireland and Williams (1974) and by Williams et
a1. (1974) over the western Atlantic Ocean averaged more than 1500 m
and often flew higher than 2000 m. These migrants may have been some
of the same types and populations of migrants tracked by Richardson.
Bruderer (1971) reported that air speeds of nocturnal migrants flying
over land varied inversely with altitude and that migrants flying at
2000-4000 m averaged air speeds of about 16 mps, a rate faster than
most passerines. Bruderer and Steidinger (1972) concluded that shore-
birds and waterfowl fly higher than small passerines, as reported by
other researchers (Bellrose, 1967; Richardson, 1971, 1972; Blokpoel and
Burton, 1975).
The altitude of migrating waterfowl varies from 1 m to >3500 m
(Appendix II). Scoters and some other ducks change altitude when
flying over land and water in a manner that is the opposite of passerine
behavior. Over water, these ducks often fly at <30 m, whereas over land
they sometimes fly above the range of unaided vision (Alerstam et a1.,
1974). Flocks of geese migrating in daylight often fly at only 100-400 m
above the ground (Wege and Raveling, 1984), but there are numerous
reports of swans, ducks, and geese flying above 1500 m (Appendix II).
A finding that seems to be universal among powered migrants is
a change of altitude with wind direction and speed. Individuals mi-
grating with opposing winds fly lower than do those flying with fol-
lowing winds (Able, 1970; Bruderer and Steidinger, 1972; Bergman,
1978; Perdeck and Speek, 1984). By flying at lower altitudes with op-
posing winds, migrants increase ground speed, thereby reducing the
cost of transport.
The altitude of soaring migrants has been studied intensively and
varies with species (Kerlinger et a1., 1985), time of day (Kerlinger and
Gauthreaux, 1984, 1985a; Kerlinger et a1., 1985), topographical con-
dition, wind direction (Kerlinger and Gauthreaux, 1984), and status in
a glide path (Kerlinger et a1., 1985). The altitude of soaring migrants
increases following takeoff in mid-morning through midday when con-
vective activity is at its maximum. At this time, hawks reach >1500 m,
although about 85% probably do not exceed 1000 m (Appendix II).
Altitude varies from moment to moment as birds glide and soar through
several hundred meters of air space, termed the height band (Kerlinger
et a1., 1985). Species of falconiforms frequently use partially powered
glides (continuously descending) and undulating (level, powered) flight
tend to fly lower than do soaring species that use soaring flight. With
opposing winds or winds lateral to the preferred migratory direction,
hawks often descend when they encounter ridges or coastlines (Ker-
linger and Gauthreaux, 1984). After descending to these "leading lines"
(Mueller and Berger, 1967) they generally fly below 100 m (Broun, 1949;
Kerlinger and Gauthreaux, 1984). Thus, wind topography, and convec-
tive activity interact to shape the altitudinal ranges used by hawks and
other soaring birds.
5. FIT OF THE DATA TO PREDICTIONS
Data pertaining to the diel timing of migration fit the predictions

made from atmospheric structure remarkably well. Most powered mi-
grants take off after sunset and land before dawn, with a peak of activity
before or near midnight. These migrants tend to be longer-distance
migrants than the diurnally migrating species. Soaring birds such as
hawks take off in mid-morning after thermal convection begins and
migrate until mid- to late afternoon when thermals dissipate.
Instances in which the diel timing of migration of powered mi-
grants does not conform ostensibly to the pattern predicted represent
exceptions that confirm the importance of atmospheric structure in the
evolution of bird migration. These include (1) some waterfowl and
shorebirds that migrate throughout the day, (2) the takeoff of some
shorebirds 2-3 hr before sunset, (3) the morning flight of some passer-
ines, (4) the diurnal migration of some passerines, and (5) the midday
migration of hummingbirds. At the very least, most fly at times of the
day, season of the year, or heights at which temperature, wind, and
turbulence are not unfavorable for migration. Waterfowl that fly at mid-
day, for example, may do so in late autumn or early spring, when
daytime temperatures are low and thermal convection is minimal. Re-
member, the boundary layer is not as deep in late autumn, winter, and
early spring as in the rest of the year, nor do thermals form as frequently
(see Fig. 2). At times loons (Kerlinger, 1982) and waterfowl (Bellrose,
1971) fly above the boundary layer, thereby avoiding thermally induced
turbulence. Furthermore, the relatively large ratio of air speed to wind
speed of these birds (as opposed to passerines and other small birds)
makes them less susceptible to turbulence effects. Many of the cases
in which shorebirds took off 2-3 hr before sunset were of migrants
initiating long flights over water (Richardson, 1979). As such, they
probably flew in cool laminar air.
The "morning flight" of passerines that are typically nocturnal
migrants and the diurnal migrations of passerines appear inconsistent
with predictions of our hypothesis. Actually, these flights occur in the
early morning before the atmosphere becomes warmer and thermal
convection develops, and in the late afternoon after the warmest and
most turbulent period has past. The term "diurnal migrant" in this case
is a misnomer because many of these birds initiate migration before

sunrise. Thus, early morning migration occurs in a fairly calm and cool
atmosphere.
Finally, hummingbirds migrate during the midday period. L. Good-
rich (personal communication), who studied the fall migration of hum-
mingbirds in the northeastern United States, explained that the feeding
habits and small size of these migrants constrain their migration to
midday (d. Kodric-Brown and Brown, 1978; Gass, 1979). By feeding
early in the morning before migration and again in the late afternoon
after migration, they can acquire energy for daily flight and the period
from sunset to sunrise. The diel pattern of nectar abundance may also
influence the diel timing of migration. Our experience with these mi-
grants during spring in Louisiana indicates that they often arrive fol-
lowing a nocturnal passage across the Gulf of Mexico, probably the
longest nonstop flight faced by most hummingbirds.
Although the data presented in Appendix I are sufficient to test
the hypothesis that migrants fly at times of the day and at heights that
are conducive to efficient and rapid migration, the data are incomplete
in several respects. First, some avian taxa are either absent or poorly
represented in the migration literature. We know little about altitude
and diel timing of migration for owls, rails, grebes, swallows, swifts,
caprimulgids, night jars, pelicans, suilids, and others. Second, knowl-
edge of the flight behavior of some supposedly well-studied migrants
is limited. Third, we know almost nothing about the way powered
migrants behave when they encounter turbulence.
Raynor (1956) suggested that passerines fly on nights when tur-
bulence is minimal as is the case during inversions. Using an elegant
statistical analysis of a large radar data set, Richardson (1978) con-
cluded, as have others (Nisbet and Drury, 1968; Able, 1973), that the
relationship of migration timing to stability and turbulence is not ob-
vious. These analyses seek relationships between atmospheric structure
and behavior on a night-to-night scale. Larkin (1982) found that mi-
grants were less numerous in turbulent elements than in areas of the
atmosphere in which turbulence was absent, seemingly indicating that
birds avoid turbulence on a moment-to-moment scale. Finally, Bellrose
and Graber (1967) proposed that it was "advantageous for birds to
migrate at night when there is homogeneity in the gustiness of the air,"
but they did not suggest the time-scale on which migrants make such
decisions. If individual birds avoid flying through turbulence or flying
on nights when turbulence is present, it is likely that natural selection
has placed a premium on avoiding turbulence. Our hypothesis can be
further tested by examining the physiology, aerodynamics, and behav-

ior of birds flying in turbulent and nonturbulent air as well as in air
varying in temperature and humidity.
With respect to the altitude of migration, data are not entirely
consistent with Pennycuick's (1978) prediction that migrants should
fly as high as available oxygen allows. Powered migrants fly mostly at
altitudes below 1000 m, far below the maximum altitude at which ox-
ygen is available, i.e.; >3000 m (Tucker, 1968b). High-altitude migra-
tion does occur, usually when winds are favorable for migrants and
during daytime flight over water by passerines or over land by some
shorebirds and waterfowl. Such migration is often above the convective
layer in cooler laminar air than near the surface.
Migration at low altitudes, especially by passerines at night or early
in the morning, may be beneficial because strong winds aloft may blow
them off course, as suggested by Able (1970), and because relative
humidity decreases with altitude, increasing the rate of evaporation.
The prediction that larger birds such as ducks and shorebirds fly higher
than passerines was upheld. Finally, the altitude of soaring birds was
found to correspond to predictions, with the exception of migrants that
used wind generated updrafts along ridges flew close to the surface.
The latter group may avoid being drifted by descending to altitudes at
which potentially drifting winds are absent. Furthermore, by using low-
altitude orographic updrafts, they can migrate when thermal convection
is absent or scarce.
The paucity of data on the diel timing and height of migration
precludes a more thorough test of the atmospheric hypothesis and can
be remedied only by rigorous studies of migrants. The strategy adopted
by most students of avian migration has been to collect data regarding
only one aspect of migration such as orientation, altitude, or flight speed
at a given location. No studies have specifically addressed the rela-
tionship between selection of altitude and diel timing of migration for
any given species. Thus, we know little about the flight strategies (sensu
Alerstam, 1981) of individual migrants. The best technique for studying
such relationships is radiotelemetry of individual migrants throughout
an entire migration or a major portion of one (ef. Cochran and Kjos,
1985). A telemetry study conducted properly would provide informa-
tion as to the precise decisions of individual birds of known age, sex,
and origin. Such studies would be expensive and difficult to conduct
but would yield precise data elucidating the flight strategies of indi-
vidual migrants and permitting more detailed tests of the hypothesis
that atmospheric conditions is a primary selective force shaping the
evolution of diel timing of migration.
ATMOSPHERIC STRUCTURE AND MICRA TION 129
6. THE DAYTIME FEEDING AND PREDATOR-AVOIDANCE

HYPOTHESES
We do not wish to imply that atmospheric structure is the only

selective force shaping the diel timing of avian migration. In addition
to atmospheric structure, two other selective forces have been proposed.
By flying at night, migrants avoid avian predators and devote daylight
hours to replenishing metabolic resources used during migration. Nei-
ther of these hypotheses can be tested using the data presented in this
chapter. We present logical arguments, however, that contradict the
predator-avoidance hypothesis and support the diurnal feeding hy-
pothesis.
Birds that fly at night are likely to be preyed upon, but it is doubtful
that predation is a strong enough selective force to be responsible for
the evolution of such a widespread behavior as nocturnal migration.
We pose two questions that obviate the predator-avoidance hypothesis:
(1) If predator avoidance was a strong selective force in the evolution
of nocturnal migration, why do so many small passerines migrate early
in the day when they are susceptible to predation by bird eating hawks
and falcons? (2) Why do large fast migrants, such as waterfowl and
shorebirds that are not preyed upon during flight, migrate at nighf? At
best, predation on migrants flying in daylight was, and is, a selective
force that worked synergistically with more effective forces.
The diurnal feeding hypothesis has greater merit than the predator-
avoidance hypothesis and, in concert with atmospheric structure, is a
potent selective force. Earlier we stated that long-distance migrants fly
at night more often than do short-distance migrants. This argument was
used to suggest that there is greater selective pressure on long-distance
migrants. As migration distance increases, the need to store fuel for
flight becomes more important. Therefore, there is a need to feed for
extended periods. Although some shorebirds (Dugan, 1981; Wood, 1986)
and waterfowl (P. Kerlinger and S. A. Gauthreaux, unpublished data)
forage at night, they do not have this option if they must fly long
distances. Short-distance migrants do not need to store massive fat
deposits and can forage during the portion of the day or on days when
they are not migrating. Long-distance and middle-distance passerine
migrants make stopovers of 1-5 days during migration to replenish fat
deposits (e.g., Cherry, 1982; Bairlein, 1985; Biebach et 01.,1986; Moore
and Kerlinger, 1987) implicating the necessity for long periods of day-
light in which to forage during the migration season. For these reasons,
we conclude that the need to forage during daylight is an important
selective force in the migration of nocturnal migration.
We argue that both atmospheric structure and the need to forage

during daylight hours are the primary selective forces that shaped the
diel timing of migratory flight. The three hypotheses should not be
viewed as competing or alternative hypotheses but rather should be
considered as synergistic (sensu Hilborn and Stearns, 1982). Together
they have shaped the diel timing of bird migration. With respect to the
height at which migrants fly, atmospheric structure has been the pri-
mary selective force.
7. SUMMARY
Three hypotheses have been proposed to explain the diel timing

of migration. The hypotheses relate to (1) the need to feed during day-
light, (2) the avoidance of predators, and (3) the structure of the at-
mosphere. We present evidence that supports the atmospheric hypoth-
esis. Local and microscale meteorological data from two locations in
North America were analyzed to generate predictions as to the optimal
time of day and altitudinal strata for migrants. Four characteristics of
the nocturnal atmosphere make migration more favorable for powered
migrants than during daylight:
1. Night air temperatures during the migration season are cooler
than at midday, which along with higher relative humidity pro-
motes convective cooling and prevents loss of body water by
evaporation. In addition, generation of lift in cool, dense air is
energetically less costly than in warm air.
2. Horizontal winds at midnight are slower than at noon so birds
are not as likely to be blown off course at night.
3. Winds at night are less variable in direction than are winds at
midday as a result of decreased thermal generated turbulence.
4. Vertical wind currents caused by thermal convection are absent
at night and shortly after dawn, which also alleviates the need
to change heading and air speed constantly. Flight by powered
migrants in turbulent air is costly because birds must adjust air
speed and heading constantly to maintain a straight and level
track over the ground.
Together, these factors promote a faster and more economical migration
at night than at midday.
A literature review of air speed, altitude, and diel timing of pas-
serine, waterfowl, shorebird, and soaring bird migration provides sup-
port for the atmospheric hypothesis. In general, birds that use powered
flight migrate at night or early in the morning (before 1000 hr), and
soaring migrants fly at midday. Large fast-powered migrants, such as
waterfowl and some shorebirds, are more likely to fly in daytime than
are small passerines, especially during late autumn or early spring,
when temperatures are cooler and less turbulence is present. These
same migrants are also more likely than small birds to fly at high al-
titudes, where winds are stronger. We conclude that atmospheric struc-
ture has been a major selective force in the evolution of diel timing and
altitude of migration and that the need to feed in daylight reinforced
this behavior.
APPENDIX I
Diel Timing of Migration
Bird group Takeoff (T) - Peak (P) - Landing (L)

with method of study Reference
Passerines
Nocturnal migrants
T = "soon after nightfall," P = 2100-2200 hr,
radar Lack (1960a,b, 1963)
T = 1800-1900 hr, P = 2200-0100 hr, radar Bellrose (1967)
T = 38-39 min after sunset, radar Parslow (1968)
T = variable, depending on wind, radar Hassler et 01. (1963)
T = 40-45 min after sunset, visual observations
with ceilometer Hebrard (1971)
T = 30-45 min after sunset, radar Richardson (1971, 1972)
T = 30-45 min after sunset, radar, P = 1.5-2.5
hr later (2000-2100 hr) Gauthreaux (1972)
P = 1845-1900 and after 2400 hr, radar,
Erithacus, Sylvia, Turd us, Regulus,
Troglodytes Alerstam (1972)
T = 32 min after sunset, P = 2 hr after sunset,
radar, Turdus spp. Alerstam (1976)
P = 2200-2400 hr, moonwatch Lowery (1951)
P = 2300-0100 hr, radar Graber and Hassler (1962)
P = 2100-2400 hr, radar Graber (1968)
P = 2.5-4 hr after sunset, radar Nisbet (1963)
T = after dark, P = 2100-2400 hr, descent after
2400", radar B1okpoel and Burton (1975)
Nocturnal migrants
Morning flight
T = shortly after sunrise, L = 4 hr after sunrise,
visual observations Gauthreaux (1978)
T = 30 min after sunrise, L = 2.5, hr after
sunrise, visual observations Bingman (1980)
(continued)

T = 1 hr after sunrise until 1000 hr, visual

observations Hall and Bell (1981)
Diurnal migrants
T = dawn or "soon after," visual observations,
P = 0800-1000 hr Lack and Lack (1952)
T = before dawn (0500 hr), L = before 1000,
Corvus, Columba (not a passerine) Fringilla,
radar and visual observations Mascher et a1. (1962)
T = <30 min before sunrise, L = 1000 hr, radar Lack (1963)
L = before 1100 hr, second P = after 1500 hr,
Sturn us, Fringilla, radar and visual
observations Alerstam and Ulfstrand (1972)
T = 43 min before sunrise, P = 1-2 hr later,
L = before 1100, many species, radar and
visual observations Alerstam and Ulfstrand (1975)
All day, Columba, radar and visual observations Alerstam and Ulfstrand (1974)
Shorebirds
T = 2 hr before sunset, 1 hr after dawn, radar Lack (1960a,b, 1963)
T = up to 2 hr before sunset, radar Drury and Keith (1962); Lack
(1962, 1963); Lee (1963);
Evans (1968); Richardson
(1972, 1979); Grimes (1974)
T = after sunset (0.5-1.0 hr), radar Swinebroad (1964); Casement
(1966); Evans (1968);
Grimes (1974); Richardson
(1979)
T = sunrise, overwater, radar Lack (1962, 1963); Lee (1963)
P = late afternoon and morning, visual
observations Theile (1970); Edelstam
(1972); Ulfstrand et a].
(1974)
P = 1845-2100 hr, radar Alerstam (1972)
Waterfowl
All day and night, visual observations, Anas,
Oxyura, Aythya, Bucephela Bellrose and Sieh (1960)
P = 1845-2100 hr, radar Alerstam (1972)
P = 2200-2400 hr, some in daytime, radar Beason (1978)
P = sunset to midnight, radar Flock and Bellrose (1970)
Soaring birds
T = about 1000 hr, P = 1200-1400 hr, L = after
1400 hr, aircraft and radar, Grus Pennycuick et a/. (1979)
T = 0800-0900 hr, P = midday, L = 1700-1800
hr, visual observations, many raptor species Evans and Lathbury (1973)
(continued)

T = 0730-0830, L = 1700-1715 hr, visual

observations, Buteo Smith (1980)
T = variable: 0800-1000 hr, 1-3 hr after sunrise,
L = 1600 hr-sunset, radar and visual
observations, Buteo Kerlinger and Gauthreaux
(1985a)
T = 1000-1200 hr, radar, Grus Beason (1978)
T = 0630-0900 hr, L = 1600-1800 + hr, visual
observations, Grus (powered flight?) Kessel (1984)
P = 0700-1000 hr, visual observations, varied by
species, Buteo, Accipiter, late-afternoon Falco Mueller and Berger (1973)
"Indicates sample may include some shorebirds.
APPENDIX II
Altitude of Migration
Bird group Altitude (m), methods, and comments Reference
Passerine
Nocturnal migrants
<300, tower kill Brewer and Ellis (1958)
300-1300-daytime, 900-1800-night, radar, over
water Adams (1962)
80% below 760, radar Eastwood and Rider (1965)
50-100% below 1500, variable, radar Bellrose (1967)
>75% below 915, radar Able (1970)
50% 150-310, aircraft Bellrose (1971)
244-488, radar, at night over water 1220-1524
in daytime over water Gauthreaux (1972)
1000-2000", radar, over water Williams et a1. (1972)
mode <610, radar Richardson (1972)
>1500", radar, over water Hilditch et al. (1973)
not above 1500, radar Houghton (1974)
x = 1627", radar, over water Ireland and Williams (1974)
80% below 2000-3500", radar, various locations,
over water Williams et a1. (1974)
maximum nightly = 1400-3780", radar Blokpoel and Burton (1975)
<500, tower kill Seets and Bohlen (1977)
65% below 400, radar McCrary et a1. (1983)
<380, tower kill Crawford (1984)
Nocturnal migrants
Morning flight
(continued)

<40, visual observations S. A. Gauthreaux, personal
communication
15-50, visual observations Bingman (1980)
<50 m, visual observations Hall and Bell (1981); G. A.
Hall (personal
communication)
Diurnal migrants
most below 300, visual observations Rudebeck (1950)
16-30, visual observations, FringilJa, Sturnus,
Alauda Lack and Lack (1952)
Beyond visual range with following winds, low
with opposing winds, radar and visual
observations, Alauda, Anthus, Carduelis,
Corvus, Turdus Wilcock (1964)
<200, radar and visual observations Mascher et a1. (1962)
80% below 1070, radar, Fringilla, Sturn us Eastwood and Rider (1965)
10-50% equal or below 200, radar and visual
observations, and Fringilla, Alauda Rabol (1967); Rabol and
Hindsbo (1972)
500-1000, radar (Columba, not passerines) Alerstam and Ulfstrand (1974)
Shorebirds
200-500, radar and visual observations,
Numenius, Vanellus, others Mascher et a1. (1962)
Beyond visual range with following winds, low
with opposing winds, radar and visual
observations, Vanellus Wilcock (1964)
1000-3000, radar, over water Williams et a1. (1972)
<3700, radar, mostly over water, Tringa,
Charadrius, Calidris Myres and Apps (1973)
>1500, radar, over water Hilditch et a1. (1973)
x = 1627, radar, over water Ireland and Williams (1974)
x = 1300, radar Richardson (1972)
2000-4000, radar, over land and water Richardson (1976)
x = 2000 (max = 6650) radar Richardson (1979)
Waterfowl
30-60, poor visibility, visual observations; <1,000,
good visibility, Anas, Oxyura, Aythya,
Bucephela Bellrose and Sieh (1960)
600-1400 radar, daytime Bellrose (1966)
400-1300 (max 2000-3000), radar, Clanqula,
Melanitta Bergman and Donner (1971)
<30, visual observations, over water above visible
range, radar, over land, Somateria Alerstam et a1. (1974)
100-2440, aircraft radiotelemetry, Cygnus, variable Sladen et a1. (1974)
(continued)
Maximum nightly = 3780, radar Blokpoel and Burton (1975)

500-2000, radar Beason (1978)
800-2000, radar, calm; 800-1200, opposing wind,
Cygnus, Anser, Branta, Clangula, Melanitta Bergman (1978)
Mostly <10, over water, maximum = 500, visual
observations, Somateria, Melanitta, Clangula Johnson and Richardson
(1982)
900-2200, radar, Gavia Kerlinger (1982)
500-600, radiotelemetry, Branta Wege and Raveling (1984)
<30, visual observations, over water Gavia J. Cherry (personal
communication)
Soaring birds
<100, visual observations, raptars, ridge gliding Broun and Goodwin (1943)
<1525, visual observations, rap tars Haugh (1972)
90% below 1370, x = 750-850, radar, raptars,
over water Houghton (1974)
Beyond unaided human vision, rap tars , over
water, radar Evans and Lathbury (1973)
>450-light winds; <60-strong winds, visual
observations, rap tars (Pernis) Beaman and Galea (1974)
300-900 +, visual observations, Grus Kessel (1984)
500-1000, radar, Grus Alerstam (1975)
<100, early and late in day, raptars, visual
observations, over water; very high at midday Finlayson et a1. (1976)
400-1200 changing constantly, radar, aircraft, and
visual observations, Grus, thermal soaring Pennycuick et a1. (1979)
<1434, aircraft, Buteo, Accipiter, thermal soaring Hopkins et a1. (1979)
Daily means (midday)-<50-737, radar, Accipiter,
thermal soaring, changing constantly Kerlinger and Gauthreaux
(1984)
x = 746-839, radar, 9 species, Buteo, Accipiter,
Falco, Circus, Pandion, thermal soaring,
changing constantly, height band = 200-400 m Kerlinger et a1. (1985)
x = 531-745, radar, 6 species Buteo, Accipiter,
Falco, ktinia, thermal soaring, changing
constantly, height band = 450 m Keriinger and Gauthreaux
(1985a,b)
"Indicates sample may include some shorebirds.
ACKNOWLEDGMENTS. Research support during preparation of this

manuscript was provided by grant BNS 8316781 from the National
Science Foundation (F.R.M.) and the University of Southern Missis-
sippi. We thank R. Cipriano, S. A. Gauthreaux, Jr., and N. Tumosa for
helpful discussion of our ideas. Comments on this manuscript by
136 PAUL KERLlNGER and FRANK R. MOORE
D. R. Griffin, G. D. Schnell, F. Bairlein, D. M. Power, D. E. Loria, and

A. ]. Kuenzi were most helpful.
REFERENCES
Able, K. P., 1970, A radar study of the altitude of nocturnal passerine migration, Bird-
Banding 41:282-290.
Able, K. P., 1973, The role of weather variables and flight direction in determining the
magnitude of nocturnal bird migration, Ecology 54:1031-1041.
Able, K. P., 1974, Wind, track, heading, and the flight orientation of migrating songbirds,
in: The Biological Aspects of Bird/Aircraft Collision Problems (S. A. Gauthreaux,
Jr., ed.), Air Force Office of Scientific Research, Clemson, South Carolina, pp.331-357.
Able, K. P., 1980, Mechanisms of orientation, navigation, and homing, in: Animal Mi-
gration, Orientation, and Navigation (S. A. Gauthreaux, Jr., ed.), Academic, New
York, pp. 283-373.
Adams, D. W. H., 1962, Radar observations of bird migration in Cyprus, Ibis 104:133-146.
Alerstam, T., 1972, Nocturnal bird migration in Skane, Sweden, as recorded by radar in
autumn 1971, Ornis Scand. 3:141-151.
Alerstam, T., 1975, Crane Grus grus migration over sea and land, Ibis 117:489-495.
Alerstam, T., 1976, Nocturnal migration of thrushes (Turdus spp.) in southern Sweden,
Oikos 27:457-475.
Alerstam, T., 1981, The course and timing of bird migration, in: Animal Migration
(D. J. Aidley, ed.), Cambridge University Press, New York, pp. 9-54.
Alerstam, T., and Ulfstrand, S., 1972, Radar and field observations of diurnal bird mi-
gration in Sweden, Autumn 1971, Ornis Scand. 3:99-139.
Alerstam, T., and Ulfstrand, S., 1974. A radar study of the autumn migration of wood-
pigeons Columba palumbus in southern Sweden, Ibis 116:522-542.
Alerstam, T., and Ulfstrand, S., 1975, Diurnal migration of passerine birds over south
Sweden in relation to wind direction and topography, Ornis Scand. 6:135-149.
Alerstam, T., Bauer, C. A., and Roos, G., 1974, Spring migration of Eiders Somateria
mollissima in southern Sweden, Ibis 116:194-210.
Bairlein, F., 1985, Body weights and fat deposition of Palaearctic passerine migrants in
the central Sahara, Oecologia 66:141-146.
Balachandran, N. K., and Donn, W. L., 1964, Short- and long-period gravity waves over
northeastern United States, Mthly Weather Rev. 92:423-426.
Baker, R R, 1978, The Evolutionary Ecology of Animal Migration, Holmes & Meier, New
York.
Beaman, M., and Galea, C., 1974, The visible migration of raptors over the Maltese Islands,
Ibis 116:419-431.
Beason, R C., 1978, The influences of weather and topography on waterbird migration
in the southwestern United States, Oecologia 32:153-160.
Bellrose, F. C., 1966, Orientation in waterfowl migration, in: Animal Orientation and
Navigation (R M. Storm, ed.), Oregon State University Press, Corvallis, pp. 73-99.
Bellrose, F., 1967, Radar in orientation research, in: Proceedings of the Fourteenth In-
ternational Ornithology Congress, pp. 281-309.
Bellrose, F., 1971, The distribution of nocturnal migrants in the air space, Auk 88:
397-424.
Bellrose, F., and Graber, R R, 1963, A radar study of the flight direction of nocturnal
migrants, Proceedings of the Thirteenth International Ornithology Congress, pp.

362-389.
Bellrose, F., and Sieh, J. G., 1960, Massed waterfowl flights in the Mississippi Flyway,
1956 and 1957, Wilson Bull. 72:29-59.
Bergman, G., 1978, Effects of wind conditions on the autumn migration of waterfowl
between the White Sea area and the Baltic region, Oikos 30:393-397.
Bergman, G., and Donner, K. 0., 1971, Wind drift during spring migration of Common
Scoter (Melanitta nigra) and the Long-tailed Duck (Clangula hyemalis!, Die Vogel-
warte 26:157-159.
Berthold, P., 1975, Migration control and metabolic physiology, in: Avian Biology, Vol.
5 (D. S. Farner and J. R. King, eds.). Academic, New York, pp. 77-128.
Biebach, H., Friedrich, W., and Heine, G., 1986, Interaction of bodymass, fat, foraging
and stopover period in trans-Sahara migrating passerine birds, Oecologia 69:370-379.
Bingman, V. P., 1980, Inland morning flight behavior of nocturnal passerine migrants in
eastern New York, Auk 97:465-472.
Blem, c., 1980, The energetics of migration, in: Animal Migration, Orientation, and
Navigation (S. A. Gauthreaux, Jr., ed.). Academic, New York, pp. 175-224.
Blokpoel, H., and Burton, J., 1975, Weather and height of nocturnal migration in eastcen-
tral Alberta: A radar study, Bird-Banding 46:31-328.
Brewer, R., and Ellis, J. A., 1958, An analysis of migrating birds killed at a television
tower in east-central Illinois, Sept. 1955-May 1957, Auk 75:400-414.
Brewster, W., 1886, Bird Migration, Memoirs Nuttall Ornithological Club 1, Nuttall Or-
nithological Club, Cambridge, Massachusetts.
Broun, M., 1949, Hawks Aloft; The Story of Hawk Mountain, Dodd, Mead, New York.
Broun, M., and Goodwin, B. V., 1943, Flight-speeds of hawks and crows, Auk 60:487-492.
Bruderer, B., 1971, Radar beobachtungen uber den Fruhlingszug im Schweizerischen
Mittelland, Ornithol. Beob. 68:89-158.
Bruderer, B. and Steidinger, P., 1972, Methods of quantitative and qualitative analysis
of bird migration with a tracking radar, NASA Spec. Publ. 262:151-167.
Casement, M. B., 1966, Migration across the Mediterranean observed by radar, Ibis 108:
461-491.
Cherry, J. D., 1982, Fat deposition and length of stopover of migrant White-crowned
Sparrows, Auk 99:725-732.
Cipriano, R. J., 1975, Sailplane measurements of planetary boundary layer structure,
M. S. thesis, State University of New York, Albany.
Cipriano, R., and Kerlinger, P., 1985, Estimating the altitude of hawk migration, in:
Proceedings of the Fourth Hawk Migration Conference (M. Harwood, ed.). Hawk
Migration Association of North America, Washington, D.C., pp. 67-73.
Cochran, W. W., 1985, Ocean migration of Peregrine Falcons: Is the adult male pelagic?
Proceedings of the Fourth Migration Conference (M. Harwood, ed.). Hawk Migration
Association of North American, Washington, D.C., pp. 223-237.
Cochran, W. W., Montgomery, G. G., and Graber, R. R., 1967, Migratory flights of Hy-
locichla thrushes in spring: A radiotelemetry study, Living Bird 6:213-225.
Cochran, W. W., and Kjos, C. G., 1985, Wind drift and migration of thrushes: A tPiemetry
study, Ill. Nat. Hist. Bull. 33:297-330.
Cone, C. D., Jr., 1962, Thermal soaring of birds, Am. Sci. 50:180-209.
Crawford, R. 1., 1984, Patterns of spring and fall migration in Northwest Florida, J. Field
Ornithol. 55:196-203.
Dawson, W. R., 1982, Evaporative losses of water by birds, Compo Biochem. Physiol.
71A:495-509.
Dorst, J., 1962, The Migration of Birds, Houghton Mifflin, Boston.

Drury, W. H., and Keith, J. A., 1962, Radar studies of songbird migration in coastal New
England, Ibis 104:449-489.
Dugan, P. J., 1981, The importance of nocturnal foraging in shorebirds: A consequence
of increased invertebrate prey activity, in: Feeding and Survival Strategies of Es-
tuarine Organisms (N. V. Jones and W. J. Wolff, eds.), Plenum, New York, pp. 101-125.
Eastwood, E., and Rider, G. C., 1965, Some radar measurements of the altitude of birds
flight, Br. Birds 58:393-426.
Edelstam, C., 1972, The visible migration of birds at Ottenby, Sweden, Var Fagelv. Supp!.
7:1-360.
Evans, P. R, 1968, Autumn movements and orientation of waders in northeast England
and southern Scotland, studied by radar, Bird Study 15:53-64.
Evans, P. R, and Lathbury, G. W., 1973, Raptor migration across the Straits of Gibraltar,
Ibis 115:527-585.
Finlayson, J. C., Garcia, E. F. J., Mosquera, M. A., and Bourne, W. R P., 1976, Raptor
migration across the Strait of Gibraltar, Br. Birds 69:77-87.
Flock, W. L., and Bellrose, F. C., 1970, Radar detection of birds: A radar study of bird
migration in the central United States, in: Proceedings of the World Conference on
Bird Hazards to Aircraft (S. A. Gauthreaux, Jr., ed.), Air Force Office of Scientific
Research, Clemson, South Carolina, pp. 273-283.
Gass, C. L., 1979, Territory regulation, tenure, and migration in rufous hummingbirds,
Can. J. Zool. 57:914-923.
Gauthreaux, S. A., Jr., 1971, A radar and direct visual study of passerine spring migration
in southern Louisiana, Auk 83: 361-367.
Gauthreaux, S. A., Jr., 1972, Behavioral responses of migrating birds to daylight and
darkness: A radar and direct visual study, Wilson Bull. 84:136-148.
Gauthreaux, S. A., Jr., 1978, Importance of the daytime flights of nocturnal migrants:
Redetermined migration following displacement, in: Animal Migration, Navigation
and Homing (K. Schmidt-Koenig and W. T. Keeton, eds.), Springer-Verlag, Berlin,
pp.219-227.
Graber, R R, 1968, Nocturnal migration in Illinois-Different points of view, Wilson
Bull. 80:36-71.
Graber, R R, and Hassler, S. S., 1962, The effectiveness of aircraft-type (APS) radar in
detecting birds, Wilson Bull. 74:367-380.
Griffin, D. R, 1969, The physiology and geophysics of bird navigation, Q. Rev. BioI. 44:
255-276.
Griffin, D. R, 1973, Oriented bird migration in or between opaque cloud layers, Proc.
Am. Phil. Soc. 117:117-141.
Grimes, L. G., 1974, Radar tracks of palaearctic waders departing from the coast of Ghana
in spring, Ibis 116:165-171.
Hall, G. A., and Bell, R K., 1981, The diurnal migration of passerines long as Appalachian
ridge, Am. Birds 35:135-138.
Hardy, K. H., and Katz, 1., 1969, Probing the clear atmosphere with high resolution radars,
Proc. IEEE 57:468-488.
Hardy, K. H., and Ottensten, H., 1969, Radar investigations of convective patterns in the
clear atmosphere, J. Atmos. Sci. 26:666-672.
Hart, J. S., and Roy, O. Z., 1966, Respiratory and cardiac responses to flight in pigeons,
Physiol. Zool. 39:291-306.
Hassler, S. S., Graber, R R, and Bellrose, F. C., 1963, Fall migration and weather: a radar
study, Wilson Bull. 75:56-77.
Haugh, J. R., 1972, A study of hawk migration in eastern North America, Search 2:1-60.
Hebrard, J. J., 1971, The nightly initiation of passerine migration in spring: A direct visual
study, Ibis 113:8-18.
Hilborn, R., and Stearns, S. c., 1982, On inference in ecology and evolution biology: The
problem of multiple causes, Acta Biotheor. 31:145-164.
Hilditch, C. D. M., Williams, T. C., and Nisbet, I. C. T., 1973, Autumnal bird migration
over Antigua, W. I., Bird-Banding 44:171-179.
Hooke, W. H., and Jones, R. M., 1986, Dissipative waves excited by gravity-wave en-
counters in the stably stratified planetary boundary layer, J. Atmos. Sci. 43:2048-2061.
Hopkins, D., Mersereau, G. S., Mitchell, J. B., Roberts, P. M., Robinson, L. J., and Welch,
W. A., 1979, Motor-glider and cine-theodolite study of the 1979 fall Broad-winged
Hawk migration in southern New England, Connecticut Audubon Council, Tariff-
ville, Connecticut.
Houghton, E. W., 1974, Highlights of the NATO-Gibraltar bird migration radar study.
Bird Strike Committee Europe Report, Paris, 1973, Royal Radar Establishment, London.
Ireland, L. c., and Williams, T. c., 1974, Radar observations of bird migration over
Bermuda, in: Proceedings of the Conference on Bird/Aircraft Strike Hazard (S. A.
Gauthreaux, Jr., ed.). Air Force Office of Scientific Research, Clemson, South Carolina,
pp. 383-408.
Johnson, C. G., 1969, Migration and Dispersal of Insects by Flight, Methuen, London.
Johnson, S. R., and Richardson, W. J., 1982, Waterbird migration near the Yukon and
Alaska coast of the Beaufort Sea. II. Moult migration of sea ducks in summer. Arctic
35:291-301.
Kerlinger, P., 1982, The migration of Common Loons through eastern New York, Condor
84:97-100.
Kerlinger, P., and Gauthreaux, S. A., Jr., 1984, Flight behaviour of sharp-shinned hawks
during migration. I. Over land, Anim. Behav. 32:1021-1028.
Kerlinger, P., and Gauthreaux, S. A., Jr., 1985a, Seasonal timing, geographic distribution
and flight behavior of Broad-winged Hawks during spring migration in south Texas:
A radar and visual study, Auk 102:735-743.
Kerlinger, P., and Gauthreaux, S. A., Jr., 1985b, Flight behavior of rap tors during spring
migration in south Texas studied with radar and visual observations, J. Field Or-
nitho1. 56:394-402.
Kerlinger, P., Bingman, V. P., and Able, K. P., 1985, Comparative flight behaviour of
migrating hawks studied with tracking radar during autumn in central New York,
Can. J. Zoo1. 63:755-761.
Kessel, B., 1984, Migration of Sandhill Cranes, Grus canadensis, in east-central Alaska,
with routes through Alaska and western Canada, Can. Field-Nat. 98:279-292.
Kodric-Brown, A., and Brown, J. H., 1978, Influence of economics, interspecific com-
petition, and sexual dimorphism on territoriality of migrant rufous hummingbirds,
Ecology 59:285-296.
Konrad, T. G., 1970, The dynamics of the convective process in clear air as seen by radar,
/. Atmos. Sci. 27:1138-1147.
Konrad, T. G., and Brennan, J. S., 1971, Radar observations of the convective process in
the clear air-A review, Aero-Revue 46:425-489.
Lack, D., 1960a, The height of bird migration, Br. Birds 53:5-10.
Lack, D., 1960b, Migration across the North Sea studied by radar. 2. The spring departure
1956-1959, Ibis 102:26-57.
Lack, D., 1962, Migration across the southern North Sea studied by radar. 3. Movements
in June and July, Ibis 104:74-85.
Lack, D., 1963, Migration across the southern North Sea studied by radar. 4. Autumn,
Ibis 105:1-54.
Lack, D., and Lack, E., 1952, Visible migration at Land's End, Br. Birds 45:81-96.
Larkin, R. P., 1982, Spatial distribution of migrating birds and small-scale atmospheric
motion, in: Avian Navigation (F. Papi and H. Wallraff, eds.J, pp. 28-37. Springer-
Verlag, New York.
Lee, S. 1. B., 1963, Migration in the Outer Hebrides studied with radar, Ibis 105:493-515.
Lenschow, D. H., 1970, Airplane measurements of planetary boundary layer structure,
/. Appl. Meteor. 9:874-882.
Lincoln, F. c., 1952, Migration of Birds, Doubleday, Garden City, New Jersey.
Lowery, G. H., Jr., 1951, A quantitative study of the nocturnal migration of birds, Univ.
Kansas Publ. Mus. Nat. Hist. 3:361-472.
Manton, M. J., 1977, On the structure of convection, Boundary-Layer Meteor. 12:491-503.
Mascher, J. W., Stolt, B-O., and Wallin, 1., 1962, Migration in spring recorded by radar
and field observations in Sweden, Ibis 104:205-215.
Masman, D., and Klaassen, M., 1987, Energy expenditure during free flight in trained
and free-living Eurasian Kestrels (Falco tinnunculus), Auk 104:603-616.
McCrary, M. D., McKernan, R. 1., Landry, R. E., Wagner, W. D., and Schreiber, R. W.,
1983, Nocturnal avian migration assessment of the San Gorgonio wind resource study
area, spring 1982. Report for Research and Development, Southern California Edison,
Rosemead, California.
Moore, F. R., 1987, Sunset and the orientation behaviour of migrating birds, BioI. Rev.
62:65-86.
Moore, F. R., and Kerlinger, P., 1987, Stopover and fat by North American wood warblers
(Parulinae) following spring migration over the Gulf of Mexico, Oecologia 74:47-54.
Moreau, R. E., 1961, Problems of Mediterranean Sahara migration, Ibis 103:373-421.
Mueller, H. C., and Berger, D. D., 1967, Wind drift, leading lines, and diurnal migrations,
Mueller, H. C., and Berger, D. D., 1973, The daily rhythm of hawk migration at Cedar
Grove, Wisconsin, Auk 90:591-596.
Myres, M. T., 1964, Dawn ascent and re-orientation of Scandinavian Thrushes (Turdus
spp.) migrating at night over the northeastern Atlantic Ocean in autumn, Ibis 106:
7-51.
Myres, and Apps, R. T., 1973, Migration of birds over the south coast of China recorded
by radar, Nature (Land.) 241:552-554.
Nisbet, 1. C. T., 1955, Atmospheric turbulence and bird flight, Br. Birds 48:557-559.
Nisbet, 1. C. T., 1963, Measurements with radar of the height of nocturnal migration over
Cape Cod, Massachusetts, Bird-Banding 34:57-67.
Nisbet, 1. C. T., and Drury, W. W., Jr., 1968, Short-term effects of weather on bird migration:
A field study using multivariate statistics, Anim. Behav. 16:496-530.
Oke, T. R., 1978, Boundary Layer Climates, Wiley, New York.
Palmgren, P., 1949, On the diurnal rhythm of activity and rest in birds, Ibis 91:567-576.
Parslow, J. 1. F., 1968, The migration of passerine night migrants across the English
Channel studied by radar, Ibis 111:48-79.
Pennycuick, C. J., 1969, The mechanics of migration, Ibis 111:525-556.
Pennycuick, C. J., 1975, Mechanics of flight, in: Avian Biology, Vol. 5 (D. S. Farner and
J. R. King, eds.), pp. 1-75, Academic, New York.
Pennycuick, C. J., 1978, Fifteen testable predictions about bird flight, Oikos 30:165-175.
Pennycuick, C. J., Alerstam, T., and Larsson, B., 1979, Soaring migration of the Common
Crane Grus grus observed by radar and from an aircraft, Ornis Scand. 10:241-241.
Pennycuick, C. j., 1983, Thermal soaring compared in three dissimilar tropical bird
species Fregata magnifiscens, Pelecanus occidentalis, and Coragyps atratus, J. Exp.
BioI. 102:307-325.
Perdeck, A. c., and Speek, G., 1984, A radar study of the influence of expected ground
speed, cloudiness, and temperature on diurnal migration intensity, Ardea 72:189-198.
Rabol, j., 1967, Visual diurnal migratory movements, Dansk Ornithoi. For. Tidssk. 61:
73-99.
Rabol, j., and Hindsbo, 0., 1972, A comparison of the bird migration recorded by radar
and visible field observations in the middle of Sjaelland, Denmark, Spring 1971,
Dansk Ornithoi. For. Tidssk. 66:86-96.
Raynor, G. S., 1956, Meteorological variables and the northward movement of nocturnal
land bird migrants, Auk 73:153-175.
Richardson, W. j., 1971, Spring migration and weather in eastern Canada: a radar study,
Am. Birds 25:684-690.
Richardson, W. j., 1972, Autumn migration and weather in eastern Canada: A radar study,
Am. Birds 26:10-17.
Richardson, W. j., 1976, Autumn migration over Puerto Rico and the Western Atlantic:
A radar study, Ibis 118:309-332.
Richardson, W. j., 1978, Timing and amount of bird migration in relation to weather: A
review, Oikos 30:224-272.
Richardson, W. j., 1979, Southeastward shorebird migration over Nova Scotia and New
Brunswick in autumn: A radar study, Can. J. Zooi. 57:107-124.
Rowland, j. R, 1973, Intensive probing of the clear convective field by radar and instru-
mented drone aircraft, ]. Atmos Sci. 12:149-158.
Rudebeck, G., 1950, Studies on bird migration based on field studies in southern Sweden,
Var Fagelv. Suppi. 1:1-148.
Salt, G. W., and Zuethen, E., 1960, The respiratory system, in: Biology and Comparative
Physiology of Birds, Vol. 1 (A. j. Marshall, ed.), Academic, New York, pp. 363-409.
Seets, j. W., and Bohlen, H. D., 1977, Comparative mortality of birds at television towers
in central Illinois, Wilson Bull. 89:422-433.
Sladen, W. J. L., Cochran, W. W., and Vose, R, 1974, Spring migration of the Whistling
Swan, in: Proceedings of the Conference on Bird/Aircraft Strike Hazard (S. A. Gauth-
reaux, Jr., ed.), Air Force Office of Scientific Research, Clemson, South Carolina, pp.
233-234.
Smith, N. G., 1980, Hawk and vulture migrations in the neotropics, in: Migrant Birds in
the Neotropics (A. Keast and E. S. Morton, eds.), Smithsonian Institution Press,
Washington, D. C., pp. 51-56.
Stull, R B., 1986, An Introduction to Boundary Layer Meterology, Reidel, Boston.
Swinebroad, J., 1964, The radar view of bird migration, Living Bird 3:56-74.
Theile, T., 1970, Traekket af Strandskade (Haematopus ostralegus) fra Vest norge til Va-
dehavet, Dan. Ornithoi. Foren. Tidsskr. 64:229-247.
Torre-Bueno, j. R, 1976, Temperature regulation and heat dissipation during flight in
birds, J. Exp. BioI. 65:471-482.
Torre-Bueno, j. R., 1978, Evaporative cooling and water balance during flight in hirds, ].
Exp. BioI. 75:231-236.
Tucker, V. A., 1968a, Respiratory exchange and evaporative water loss in the flying
Budgerigar, J. Exp. BioI. 48:67-87.
Tucker, V. A., 1968b, Respiratory physiology of House Sparrows in relation to high-
altitude flight, J. Exp. BioI. 48:55-66.
Tucker, V. A., 1974, Energetics of natural avian flight, in: Avian Energetics (R A. Paynter,
ed.), Publication No. 15 of the Nuttall Ornithology Club, Cambridge, Massachusetts,

pp. 298-333.
Ulfstrand, S., Roos, G., Alerstgam, T., and Osterdahl, 1., 1974, Visible bird migration at
Falsterbo, Sweden, Var Fagelv. Supp!. 8:1-245.
Warner, J., 1970, The microstructure of cumulus cloud. Part III. The nature of the updraft,
J. Atmos. Sci. 27:682-688.
Wege, M. 1., and Raveling, D. G., 1984, Flight speed and directional responses to wind
by migrating Canada Geese, Auk 101:342-348.
Wilcock, J., 1964, Radar and visible migration in Norfolk, England: A comparison, Ibis
106:101-109.
Wilde, N. P., Stull, R. B., and Eloranta, E. W., 1985, The LCL zone and cumulus onset,
J. Climate Appl. Meteor. 24:640-657.
Williams, J. M., Williams, T. C., and Ireland, L. C., 1974, Bird migration over the North
Atlantic Ocean, in: Proceedings of the Conference on the Biological Aspects of the
Bird/Aircraft Collision Problem (5. A. Gauthreaux, Jr., ed.), Air Force Office of Sci-
entific Research, Clemson, South Carolina, pp. 359-382.
Williams, T. C., Williams, J. M., Teal, T. M., and Kanwisher, J. W. 1972, Tracking radar
studies of bird migration, NASA Spec. Publ. 262:115-128.
Wood, A. G., 1986, Diurnal and nocturnal territoriality in the Grey Plover at Teesmouth
as revealed by radio telemetry, J. Field Ornithol. 57:213-221.
Woodcock, A. H., 1975, Thermals over the sea and gull flight behavior, Boundary-Layer
Meteor. 9:63-68.
Woodward, B., 1949, The motion in and around isolated thermals, Q. J. R. Meteor. Soc.
85:144-151.
World Meteorological Organization. (Anon.), 1978, Handbook of meteorological fore-
casting for soaring flight. Tech. Note #158, World Meteorological Organization, Geneva.
Yapp, W. B., 1962, Some physical limitations on migration, Ibis 104:86-89.
CHAPTER 4
PASSERINE MIGRATION BETWEEN

THE PALAEARCTIC AND AFRICA
GABOR L. LOVEI
1. INTRODUCTION
Migration is one of the possible responses by which an organism can

react to changes in its environment. The persistence of biological pop-
ulations depends on their ability to find those conditions in space and
time under which they can survive and reproduce most successfully.
For example, seasonally favorable conditions are offered by vast areas
of the northern hemisphere. There is a premium on acquiring traits that
help to reach such areas (Southwood, 1977), and birds, among others,
have responded to this evolutionary challenge. Migration must have
evolved several times in different avian taxa over geological times (Cox,
1985), and the diversity of avian migratory systems is very wide (Gauth-
reaux, 1982).
A considerable proportion of the resources that abound during the
temperate summer is used by birds that visit the temperate zone to
breed. Billions of birds migrate in spring to the northern temperate
region and, in autumn, increased in numbers by their offspring, return
to the areas that have more benign conditions. This dynamic event of
unparalleled scale among the vertebrates involves a regular seasonal
redistribution of a considerable biomass over an area of about 4 x 10 7 km 2 •
GABOR L. LOVE! • Laboratory of Functional Ecology, Department of Zoology. Plant

Protection Institute, Hungarian Academy of Sciences, Budapest, H-1525 Hungary.
144 GABOR 1. LOVE!
About 400 species have breeding ranges in the northern temperate

region and winter in the tropics. Three major land masses, Central and
South America, Africa, and Indomalaysia, serve as major wintering
areas to birds that breed in the temperate zone (Karr, 1980).
We know much more from the Palaearctic-African and the Nearctic
migration systems than from the Palaearctic-Asian migration sys-
tem(Curry-Lindahl, 1981). It seems, however, that Africa as a wintering
area is more important for Palaearctic migrants than is India or south-
eastern Asia (Moreau, 1972; Curry-Lindahl, 1981), although by species
number there is little difference (India 115, southeast Asia 142, Africa
118 wintering species) (Karr, 1980).
The Palaearctic-African migration was treated by Moreau (1972)
and, more recently, with an emphasis on Africa, by Curry-Lindahl (1981).
These investigators provide excellent overviews of the topic but have
generated more questions than answers (Lack, 1983). This chapter re-
views the topic with an emphasis on the ecology of the migrants, con-
sidering resource fluctuations in the wintering areas, the use of these
resources, the composition and dynamics of the wintering assemblages,
and the interaction of migrants and residents. This discussion considers
passerines only; by species number (probably by number of individuals
as well), they form the majority (64-82 0/0) of the migrants in all con-
tinents (Karr, 1980).
2. LONG-TERM FLUCTUATIONS IN THE PALAEARCTIC

AND AFRICA
The glacial and interglacial periods caused large changes in the

vegetation of the Palaearctic. At the end of the last glaciation, about
18,000 years ago, very little woody vegetation existed north of the Pyr-
enees, Alps, and Caucasus mountain ranges. In the mid-Palaearctic,
tundra and wooded tundra occupied the area in which taiga (coniferous
forest) is now found. Here, about 0.5 x 106 km 2 of woodland persisted,
and the steppe occupied a larger surface of land than today (Moreau,
1972). Iberia, the Italian peninsula, and the Balkan also had some wooded
steppe and mixed woodland, but their major vegetation type was wooded
tundra.
After the decline of the glaciers, vegetation belts moved northward.
This culminated about 7000 years BP, when world temperatures were
about 2°C higher than at present; about 90% of Europe was occupied
PALAEARCTIC-AFRICAN PASSERINE MIGRATION 145
by forests. Soon after, the vegetation was increasingly modified by man,

especially in the Western Palaearctic. About one fourth of the area is
covered by woodlands today, compared to 4000 years BP, when wood-
lands covered about 6 x 106 km2, an increase of 12-fold over the wood-
land minima. Changes on this scale have occurred repeatedly during
the glacials.
The probable consequences of woodland fluctuations for Palaearc-
tic migrants are that from their lowest numbers during the glaciation,
woodland migrants expanded about 10-fold (about 5000 years BP), then
declined to 25% of this by today (Moreau, 1972). Birds breeding in
bushy and open habitats have experienced a smaller amplitude of change;
most such species could never have occupied extensive areas. Migrants
living in tundra and steppes were favored by the changes during the
glaciation and may have been more numerous than at any other time
since (Moreau, 1972).
Similar long-term climatic changes have occurred in the Nearctic,
with corresponding changes in the vegetation and shifts in the distri-
bution of migratory birds (for a review, see Gauthreaux, 1980, and
references cited therein). A major difference is that because of the
north-south direction of the high mountains in America, fewer plant
species became extinct during the last glaciation than in Europe, where
the Alps blocked the escape to the south of many species during glacial
periods.
Africa has also undergone enormous climatic changes over geo-
logical times. The glacial and the interglacial periods in the Palaearctic
and Nearctic corresponded to pluvial and interpluvial (arid) periods in
Africa. New records indicate 17 such periods over the last 1,700,000
years, 8 of which were during the last 700,000 years (Kukla, 1977).
The Sahara was a hot, humid place for 100,000s of years (Monod,
1966, cited in Curry-Lindahl, 1981). About 40,000 years ago, conditions
gradually became drier, then underwent a second moist period nearly
6000 years BP, causing profound and rapid changes in the vegetation.
The Western Sahara, for example, was a Mediterranean-type scrub but
extended about 300 miles farther south than at present. The recent
extension of the Sahara is less than 5000 years old.
In East Africa, the lowland forest-savanna is oldest on the coast
(15-25 x lOG years), but its extension has also changed repeatedly and
considerably: in the humid periods, the forest from the Congo basin
moved to the east and withdrew when arid periods occurred. About
65,000 years BP, a severe arid period nearly exterminated the Congo
rain forest.
146 GABOR L. LOVE!
3. THE AFRICAN CONTINENT: FAUNA AND RESOURCES
3.1. Faunal Relationships

On an area of 24 X 106 km2, the Afro-tropical region has 1450
breeding and 1685 total bird species (Brown et 01., 1982). Of this, Zaire
(2.345 X 106 km2) has 1086 species. The richest countries are Kenya
(811 breeding and 985 total species) and Uganda (840 breeding and
1060 total species). South America is the continent with the richest
avifauna on earth: on 17.5 X 106 km 2 there exist 2500 breeding and a
total of 2936 species (A. F. Skutch, personal communication). In South
America, Ecuador has the richest avifauna (1780 breeding and 1980
total species, Welty 1980; Pomeroy and Lewis 1987).
Pomeroy and Lewis (1987) analyzed species richness-area rela-
tionships in 18 tropical African countries and compared these with 12
tropical American relationships. They conclude that the difference is
significant if breeding species are considered (when all species are
considered, America still has more species, but the difference is not
significant). The "zone of maximum species richness" was found in
Uganda and Kenya. Data from smaller areas in the two continents showed
similar species richness, suggesting that the difference was not intrinsic
but historical. They argue that the more complex relief, the high moun-
tains and valleys in tropical South America, provided a greater degree
of geographical separation which, in turn, resulted in greater speciation.
By contrast, tropical forests in West and Central Africa are on flat terrain,
providing fewer barriers to the spread of species. This seems to hold
also for flowering plants (Raven, 1976). However, the theory of the
Pleistocene forest refugia provide an alternative and better explanation
(Pearson, 1982).
A total of 479 species and subspecies are mentioned as migrants
to Africa by Curry-Lindahl (1981). Of these, 177 breed in Europe, 89
in West and Central Asia, and 15 in East Asia. Eurasian short-distance
migrants are not included in this number. In the detailed table in his
book, Curry-Lindahl lists 135 species (214 species and subspecies) of
passerines as Palaearctic migrants to Africa. Intra-African migration is
not insignificant either and involves 532 species and subspecies of
African birds (Curry-Lindahl, 1981).
Most species of migrants to Africa belong to the families of thrushes
(Turdidae, 18 species) and warblers (Sylviidae, 29 species). Swallows
(Hirundinidae, 5 species), pipits (Motacillidae, 6 spp.), and shrikes
(Laniidae, 6 species), are also important (Karr, 1980; Curry-Lindahl,
1981). All these families (except the swallows) have fewer or no species
PALAEARCTIC-AFRICAN PASSERINE MICRA TION 147
as Neotropical migrants. Seven species of swallows and 8 species of

thrushes are Neotropical migrants. Migrant thrushes to Africa are mainly
insectivorous (not those that winter in the Mediterranean, see Section
5.1), while those of the Neotropics are frugivorous (Karr, 1980).
Warblers (family Sylviidae) make up 25% of the migrant species
in Africa and 31% in the Neotropics (Parulidae); all other passerines
are 38% and 51%, respectively (Karr, 1980). Many more finches (Frin-
gillidae) are Neotropical than Palaearctic migrants, 13 versus 3 species
(Karr, 1980). Migrants of the species-rich families of wood warblers
(Parulidae) and tyrant fly cathers (Tyrannidae) are exclusively Neotropic
migrants (46 and 23 species, respectively), as well as the vireos (Vi-
reonidae, 8 species) (Karr, 1980).
Estimates of the number of birds in Africa are scanty. Brown et al.
(1982) estimated this number at 70 x 10 9 • The number of migrants was
estimated to be between 1.6 and 5.0 x 10 9 (Moreau, 1972; Schilz, 1971).
In a more detailed evaluation, Pomeroy (1988), estimating the land bird
populations in East Africa from census data at 35 sites, calculated 23 x 109
birds. Insectivores, which make up the majority of Palaearctic passerine
migrants, contributed 50% to density and about 50% to biomass. The
contribution of migrants was fairly large in open habitats (25%) and
smaller (about 10%) in woody habitats. These latter, being small in-
sectivores, contributed little to the total biomass in woody areas (less
than 10%).
Bird densities show great seasonal fluctuations. In the Tsavo area,
which is an extension of the Somali arid belt with vegetation dominated
by bushed and wooded grassland, bird densities varied between 1.95
and 6.15/ha, showing a peak in January and a low in August-September.
Insectivore densities were between 0.83 and 2.95/ha, with a peak in
December and a minimum in June. Palaearctic migrants were absent or
at a very low density from March to October. When present, their den-
sities were 0.4-1.25 birds/ha, lowest in November and highest in De-
cember and January. The relative abundance of Palaearctic migrants
during the migration and wintering period was 29-59% (Lack, 1983,
1985).
Morel (1968) registered similar seasonal density trends in a wood-
land savanna in the Sahel, West Africa. Mean bird densities during the
3 years studied varied between 0.85/ha (May) and 5.5/ha (October), an
increase of 6.5-fold. Densities of Palaearctic birds were lowest in April
(0.6/ha) and highest in October (1.9/ha). Between September and April,
the relative abundance of Palaearctic birds among all birds varied from
31 % to 71% (0.6-1.9/ha); during winter (November-February), their
importance was 47-71 % (1.0-1.8/ha).
148 GABOR L. LOVE!
• mountains
IIiI1 rain forest
~ moist woodland
ai] savanna
o desert
[J sclerophyllous shrub
FIGURE 1. Major vegetation belts in Africa.
Seasonal fluctuations in density are greater in areas that are im-

portant as wintering grounds for Neotropical migrants. In Florida and
Bahama pine forests, Emlen (1980) found 90 birdslha in April and
160/ha during winter. In an evergreen forest in Mexico, summer density
was 1.7/ha increasing to 67/ha in winter (Hutto, 1980). These increases
probably are due to the fact that migrants from 16 x 106 km 2 of North
American breeding grounds are compressed onto 2 x 106 km 2 of win-
tering grounds (Keast, 1980).
3.2. Vegetation Belts in Africa: Their Importance to Migrants

Africa has several areas with different vegetation types of impor-
tance to migrants (Fig. 1). In the north, Mediterranean Africa is com-
posed of a narrow stretch with mainly macchia-type bushes and some
forests on the northwest, the Atlas and Rif mountains. In spring this
can be an important area as a stopover site after the trans-Saharan
crossing.
PJ\LJ\EJ\RCTIC-AFRICJ\N PJ\SSERINE MIGRATION 149
The Sahara desert covers extensive areas and in no place is nar-

rower than 1500 km. Conditions are generally more severe in the east,
where it reaches the Mediterranean Sea. In the west, the relief is more
complex. Oases cover 1 % of its surface, and it remains to be established
what role they play in the trans-Saharan crossing of migrant birds (see
Section 4.4).
South of the Sahara, in the Sahel (Sudan), dry wooded savannas
dominate. Acacias are the most abundant trees, but several species of
trees, bearing fruit in winter (e.g., Salvadora persica), are important to
migrant and wintering passerines. Further south are the Guinea savan-
nas, moist woodlands with tall grass and trees.
This zonation, which spreads across the whole continent, is more
regular in West Africa (P. J. Jones, 1985), while the highlands and
mountains in East Africa induce a great variety of vegetation types
(Moreau, 1972; Walter, 1973). Rain forests cover smaller areas in Africa
than in the Neotropics and are largely confined to the Congo Basin and
the West African coasts. From the Ethiopian highlands to the south,
acacia steppe, degenerating to semidesert in places, dominates to about
central Tanzania. From here to about 15° S, the vegetation is deciduous,
light-foliaged Brachystegia-Isoberlinia woodland (the Miombo sa-
vanna). Farther south, the pattern changes again; there is a marked
difference between the humid east and the dry west. South of the equa-
tor, desert is only formed on the coast of Southwest Africa.
Human activity, as in the Neotropics, has had far-reaching effects
on the vegetation through burning, overgrazing, cutting woody vege-
tation, and establishing new land for agricultural cultivation. This im-
pact is especially marked in the Sahel and in parts of East and Southeast
Africa.
More species winter north than south of the equator: 175 species
and subspecies winter in West Africa and 198 in Sudan, while Zim-
babwe has 75 and the Cape Province and South Africa only 58 species
(Curry-Lindahl, 1981).
Among the habitat types, the northern savannas receive the ma-
jority (223 species) of migrants. Within the sub-Saharan zone, the Sudan
is more important as a wintering area than are the West African savan-
nas (Curry-Lindahl, 1981). In West Africa, the drier savannas are more
frequented by migrants than are the more humid belts toward the south
(Morel, 1968; P. J. Jones, 1985). The role of the rain forest is not fully
understood and poorly documented. Birds probably do not avoid the
rain forest as Moreau (1972) had written. Canopy makes the activity of
small birds nearly unobservable. Curry-Lindahl (1981) reported that by
150 CABOR L. LOVE!
listening to vocalizations he was able to identify several species of

migrants in the Zairean rain forest. Even the Sahara desert, far from
being lifeless, offers wintering habitat for 15 bird species.
In the Neotropics, there is a very definite southward decline in the
numbers of wintering species and individuals, paralleled by an increase
in the number of resident species. At the northern edge of the wintering
zone, migrants dominate; in Florida and the Bahamas, the winter den-
sities are 20 times higher than summer densities (Emlen, 1980); in
Mexican rain forests, the increase is 25-fold (Hutto, 1980). On a larger
scale, 30% of birds are migrants in Mexico, about 20% in Central Amer-
ica, 24-46% in Colombia (Terborgh, 1980), and only 5-7% in lowland
rain forests further to the south (Pearson, 1975). Highlands, rain forests,
and secondary growth areas are used mainly as wintering habitats. In
contrast with Africa, grasslands/savannas are not important (Karr, 1976aJ,
probably because they are secondary habitats in Central America (Keast,
1980).
3.3. Rainfall and Resource Fluctuation Patterns

There are marked seasonal changes in the habitats important for
migrants. In the northern woodland savanna belt, which spreads from
Senegal to Sudan, the average precipitation is 1000-1250 mm/year. The
rainy season lasts from the end of April to October and the dry winter
from November to March. In West Africa, an additional important factor
is the harmattan, a dry and warm Saharan wind. The rain forests in the
Congo basin have a nine month rainy season and show less seasonality.
In equatorial East Africa, there are two rainy seasons: the "short" rains
from September to November and the "long" rains from March to June.
South of the equator, on the Miombo woodland savanna, the rainy
season overlaps with the stay of the migrants, lasting from November
to April. The warmest months are September and October.
The seasonality of the rainfall is a major governing factor in the
Guinea savanna belt and Sudan. Insect abundance is closely tied to the
rainfall. During the wet season, relative arthropod biomass on the ground
and in the grass was found to increase by a factor of 5-6 over the dry
season on the East African savanna, Tsavo National Park, Kenya (Lack,
1986a). Large arthropods were more seasonal in occurrence and were
responsible for a large proportion of the peaks and the major part of
the variance in insect biomass (Lack, 1986a). The "short" rains in No-
vember-December were more reliable than the April "long" rains. The
major peaks of food abundance (fruits, nectar, grass seeds, and arthro-
pods) were during the latter stages of each wet season, more in the
more reliable "short" wet season. Nearly all food types, however, were
available throughout the year, seeds and insects on the ground probably
being more available during poor periods than superficial appearance
might suggest.
In woody vegetation in Senegal, these differences were much larger;
in 2 years, insects were 17 and 60 times more abundant in the wet than
in the dry season (Morel, 1968). Similar differences are expected to
occur on the foliage in East Africa, too (Lack, 1983). On the Serengeti
plains, Folse (1982) found a 10-fold increase in ground- and grass-living
arthropod biomass in a woodland savanna plot between Decem-
ber-January (the end of the dry season and beginning of short rains)
and May-June (the long rains). This is a significant seasonal variability
for several arthropod groups (all arthropods, large arthropods, acridid
grasshoppers). In the open savanna, variations were five- or sixfold or
less, decreasing with greater intensity of mammal grazing (Folse, 1982).
In most areas, these seasonal variations were not significant and Folse
concluded that food availability during the dry season was better than
reported by Sinclair (1978). On the Miombo woodland savanna, fruits
are abundant in October and insects increase in density from November
to April (Curry-Lindahl 1981).
In general, conditions during the presence of Palaearctic migrants
in Africa north of the equator are good at arrival and deteriorate con-
tinuously during their stay. However, there are remarkable differences
in climatic regions. Several investigators emphasize that dry season
conditions may be less harsh than would appear at first sight (Curry-
Lindahl, 1981; Folse, 1982; Lack, 1983).
Resource abundance during the migrants' stay in the Neotropics is
also variable by places and by taxonomic groups (Janzen, 1973; Hutto,
1980; Buskirk and Buskirk, 1976). In some places and in some arthropod
taxa, the peak of abundance is in the dry season (Janzen and Schoener,
1968).
4. BEHAVIOR OF THE MIGRANTS
4.1. Regulation of Migratory Behavior

Migratory activity follows the cyclical changes in weather and re-
sources and is a periodic activity itself. This annual cycle is regulated
by a finely tuned interplay of many factors both innate and external
(see, Gwinner, 1977, and Meier and Fivizzani, 1980, for reviews).
In the Old World, the genus Sylvia is the most extensively studied,
152 CABOR L. LOVE!
owing to the work of a group at Vogelwarte Radolfzell, Germany. This

genus, with 15 to 19 species and a wide diversity of migratory behavior,
is ideal for ecophysiological studies on passerine migration (Berthold,
1988a). During 20 years, this group has studied more than 25,000 birds
in the field, and more than 1500 individuals of 11 species were hand-
raised.
It was demonstrated that circannual rhythms control all annual
events, including molt and migration. There is evidence that molt and
migratory behavior are under genetic control, and there is a close pos-
itive correlation between the amount of migratory activity and the dis-
tance to travel (Gwinner, 1968; Berthold and Querner, 1981; Berthold,
1985). Cross-breeding experiments with a migratory (Finnish) and a
resident (Azores) population of the Blackcap (Sylvia atricapilla) showed
intermediacy of the migratory activity and juvenile molt (Berthold and
Querner, 1982a).
Migratory direction is also genetically programmed; this was dem-
onstrated for the Garden Warbler (Sylvia borin) by Gwinner and
Wiltschko (1980). Garden Warblers under experimental conditions
showed a preference to fly southwest and then, after a few nights, to
fly south. This matches the direction wild-living conspecifies have to
follow to reach winter quarters in Africa. The shift to south occurred
at the time the migrants should have reached southern Spain.
The amount of migratory restlessness may be indicative of the
wintering area. A two-stage migratory activity typical for several pas-
serine migrants to Africa was indeed found in the Marsh Warbler (Ac-
rocephalus palustris) (Berthold and Leisler, 1980; Lack, 1983). In this
particular species, however, a three-step migration was found (Dowsett-
Lemaire and Dowsett, 1987), underlining the necessity of parallel ex-
perimental and field research as advocated by Berthold (1988a).
4.2. Preparation for Migration: Fattening

The main energy source during migration is accumulated fat. The
major mechanism of premigratory fattening is hyperphagia (Blem, 1980),
although changes in the efficiency of food utilization were recently
demonstrated for the Garden Warbler (Bairlein, 1985a). There are four
patterns of fat deposition before and during migration (Blem, 1980):
short-range intracontinental migrants can begin migration (1) before or
(2) after peak lipid deposition; and medium- or long-range migrants
also begin migration either (3) before or (4) after maximum lipid dep-
osition.
Many Palaearctic migrants begin migrating with nonmaximal fat
reserves. They can gradually build up fat reserves or stop at fattening

sites. Heavy birds tend to fly faster, which is more advantageous for
them (Pennycuick, 1975); fat birds are also more vulnerable to predators
(Lima, 1986), which makes slow flight and many stopovers disadvan-
tageous.
The Sedge Warbler (Aeroeepha1us sehoenobaenus) is a long-dis-
tance migrant that begins migration after maximum fat deposition. Birds
accumulate large fat reserves in southern England and northern France
and overfly Spain (Bibby and Green, 1981, 1983). A similar species,
the Reed Warbler (A. seirpaeeus) fattens in September-October in Por-
tugal (Bibby and Green, 1981). The Pied Flycatcher (Fidecu1a hypo-
1euea) also fattens on the northern coast of the Mediterranean. It es-
tablishes temporary feeding territories to catch insects (Bibby and Green,
1980); its fattening rate in Portugal was reported to be 0.34 g/day (Bibby
and Green, 1980).
However, fattening sites are not necessarily near the Mediterranean
coast for all species; Thrush Nightingales (Luscinia 1uscinia) were found
to use a stopover site in central Hungary for premigratory fattening
(Cs6rgo and L6vei, 1988). The Pennycuick method of flight-range es-
timation showed that fat reserves of the heaviest birds enabled them
to reach the Sudan in one continuous flight.
Many sylviids begin migration before maximum fat deposition,
whether a short- or long-distance migrant, at least in autumn. Garden
Warblers have a mean body mass of about 20 g in England; this grad-
ually increases toward the south and in southern Italy (Scebba et a1.,
1985) reaches a mean of 23 g, to attain a flight range necessary for a
successful Saharan crossing (Bairlein, 1987). In other sites along the
northern Mediterranean coast, however, lower body masses are com-
mon (Bairlein, 1987).
Data from premigratory fattening are more scarce from Africa. Those
available indicate a similar gain in body mass in West Africa, e.g., for
the Reed Warbler (Dowsett and Fry, 1971), the Yellow Wagtail (Mota-
eillaflava) (Wood, 1982) and other species (Fry et a1., 1968). The pattern
of premigratory fattening may be different in different regions in Africa,
as found for the Marsh Warbler (data reported in Dowsett -Lemaire and
Dowsett, 1987).
Body mass data available for a number of species from a number
of sites along their migratory route are, however, seldom detailed enough
to understand the migratory tactics individual species employ. Migrants
from the Central and East Palaearctic have to refuel repeatedly (Moreau,
1972). Many passerines arrive to the edge of the desert with insufficient
reserves to cross the Sahara. Are they doomed to perish during the
154 GABOR L. LOVE!
attempted crossing? Passerines wintering in eastern Africa do not fatten

up there before spring migration (Lack, 1983; Dowsett-Lemaire and
Dowsett, 1987); their fattening sites are unknown.
4.3. Migratory Routes

Individual populations are adapted to their particular set of con-
ditions; at the end of the journey in Africa, this results in very different
arrival-departure timetables of the same species in neighboring regions
(Curry-Lindahl, 1981). It seems, therefore, that there is no "migrant
community" as such, and Karr's (1980) cautious use of the term "mi-
grant assemblage" is preferred.
An important difference between the Palaearctic and the Nearctic
migration is the difference in the presence of geographical barriers to
migration. The only substantial barrier to Neotropical migrants is the
Gulf of Mexico. A migrant crossing the Gulf has to overcome up to
1300 km over open water, although most actual crossings are shorter
(Karr, 1980). No major desert or mountain barriers occur in the Neo-
tropics. In the Palaearctic lie extensive dry lands in the zone of the
Tropic of Cancer. Consequently, migrants have to cross vast areas of
desert and semidesert during their journeys (Fig. 2). Evidence shows
that not even small passerine migrants are deterred from crossing these
inhospitable terrains, and they do no always choose the shortest route.
The Sahara is about 1500 km wide at its narrowest. Migrants from
the Western Palaearctic must cross the Mediterranean and also the
Sahara, but no passerine species show concentrations at the short cross-
ing of the straits of Gibraltar, Sicily, or Bosphorus, as do many non-
passerines. In autumn many small passerines fly over Europe in a south-
western direction and arrive at the southwestern corner of the continent,
Cape Saint Vincent, Portugal. This cape is only 400 km northwest of
Gibraltar but from here, as a departure point, birds must make a much
longer crossing over the sea to reach the African coast, which they do
in great numbers (Moreau, 1972; Curry-Lindahl, 1981).
For several species with a wide Palaearctic breeding range, there
is a migratory divide in the west of which populations fly southwest,
while the eastern populations fly southeast (see the maps in Zink
1973-1985). For the Blackcap, this divide is at about 15° E (Klein et
a1., 1973).
In other species, such as the Red-backed Shrike (Lanius collurio),
the Wood Warbler (Phylloscopus sibilatrix) or the Lesser Whitethroat
(Sylvia curruca), migration routes supposedly reflect ancestral routes
of dispersal into the present breeding area, and all European popula-
Pi\U\EARCTIC:-AFRICAN I' ASSERINE MICRA TION 1 :15
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156 CABOR L. LOVE!
tions of these species migrate southeast and cross the Mediterranean

diagonally at its widest point. A most unusual example of this ancient
dispersal route is that of the Wheatear (Oenanthe oenanthe), which has
colonized two northern corners of the New World: Greenland, arriving
from Europe, and Alaska, arriving from Siberia. The Greenland popu-
lation migrates to the African winter quarters via Europe, while the
Alaskan population flies over Siberia and the Middle East, covering
11 ,500 km twice every year.
Early arrival in spring is advantageous, as reflected in the greater
speed of the spring migration. Consequently, many species use different
patterns of fattening and migration in spring than in autumn (Blem,
1980). Such loop migration is shown, for example, by two flycatchers.
The Pied Flycatcher and the Collared Flycatcher (F. albicollis) migrate
through Spain to West Africa in autumn but return via North Africa,
Greece, and Italy in spring (Zink, 1973-1985). The Red-backed Shrike
migrates via Sudan and Zaire to its South African winter quarters and
in spring returns through East Africa and Arabia (Curry-Lindahl, 1981).
Other such species include the northern race of the Willow Warblers
(P. trochilus acredula) and the eastern race of Bonelli's Warbler (P.
bonelli orientalis).
4.4. Overcoming Geographical Barriers

As a mechanism for trans-Saharan crossing, Moreau (1972) and
Curry-Lindahl (1981) expressed the opinion that most migrants cross
the Sahara in a continuous flight. At the northern edge of the desert,
on the Mediterranean coast, and at the end of a long hot summer, the
migrants cannot find much food with which to refuel before the Saharan
crossing. At this stage, again, there is no sign of a concentration along
the Nile river on the east, which would lead migrants into the Sudan
without the dangerous desert crossing. Species such as the Whitethroat
(Slyvia communis) and the Pied Flycatcher cross the Sahara diagonally,
embarking on a flight of about 2000 km (Curry-Lindahl, 1981).
A Saharan crossing would require a continuous flight of about
50 hr, the actual time being influenced by wind velocity and direction.
The rather rough theoretical estimates of flight range available indicate
that theoretically birds can accumulate the amount of fat necessary for
such a long flight (for reasons of flight mechanics, this can be a maxi-
mum of about 50% of a bird's body mass) (Pennycuick, 1975). Body
mass data of several species show a fattening of this extent (see Moreau,
1972, and references cited therein), with corresponding decreases in
body mass at the other end of the Sahara, both in autumn and in spring.
I'ALAEAI{CTlC-AFRICAN PASSERINE MIGRATION 157
Some species, such as the Yellow Wagtail, are on the brink of their
theoretical t1ight range (Wood, 1982). A further advance toward the
south of the Sahara may have serious negative consequences for such
long-distance migrants (Winstantley et aI., 1974).
However, recent work on migrant passerines in the Eastern (Bie-
bach, 1985, 1988; Biebach et aI., 1986) and Western Sahara (Bairlein
et a1., 1983; Bairlein, 1985b) revealed an unexpected puzzling set of
facts: (1) large numbers of passerine migrants can be caught in Saharan
oases in both lean and fat conditions; (2) fat birds are not active during
daytime and leave the following night, while the lean birds are feeding
actively, stay longer, and put on fat; (3) fat birds are attracted to small
green patches established by the researchers in the desert, resting in
the shade during the day and leaving the following night, while lean
birds are not attracted to such spots; and (4) a number of birds of
different species with high fat levels have been found resting in shaded
hiding places in the desert, sometimes in crevices or holes.
On the basis of these data, Biebach et a1. (1986) proposed the hy-
pothesis that small passerine migrants would apply an intermittent
migratory strategy and cross the Sahara in several successive one-night
flights. It is not known how many individuals of which species and for
what reason would choose this strategy, nor is it clear why this would
be advantageous. Further data are needed to understand the extent,
importance, and evolutionary benefits of this type of behavior. Breeding
experiments with a partially migrant Blackcap population showed a
surprising plasticity in the genetic control of migratory behavior (Bert-
hold and Querner, 1982b; Berthold, 1988b) suggesting it is not probable
that such intermittent strategy would be a "relict" from the times when
the Sahara was a more wet area with more lush vegetation.
Migrants that breed north-northeast of the Mediterranean Sea have
to face harsher conditions and even more complicated topography to
reach Africa than do those in Europe (Fig. 2). In their way lie the Black
and the Caspian Seas; the surrounding areas, especially in autumn, are
semideserts. North and east of the Caspian Sea, vast areas of arid land
(nearly 2 x 10 6 km 2 ) are also to be overflown. The distances to be cov-
ered here equal or surpass the Mediterranean diagonal crossing; the
few records note very harsh conditions but mention several species of
passerine migrants on their way to Africa (Gladkov, 1957).
Migrants originating in the Eastern Palaearctic must cover immense
distances. It would not be surprising if they choose to fly the shortest
distance, by great circle. A few such routes are indicated in Fig. 2.
Distances of 6000-10,000 km from eastern Siberia to Lake Chad or
Kenya. There is some evidence that birds indeed fly along these tra-
158 GABOR 1. LOVE!
jectories, which include wide stretches of permanent desert or areas in

the Middle East (Iran, Iraq, Arabia) which, in autumn, are in a semi-
desert condition.
Another great circle route would lead Eastern Palaearctic migrants
over Tibet, Punjab, and the Indian Ocean. There is no indication of the
intensity of bird migration over Tibet. All available data, which are
scanty, indicate intensive migration over the Indian Ocean, in autumn
at least (Moreau, 1972; Curry-Lindahl, 1981). This is aided by a north-
east monsoon wind, but the distance of the ocean crossing, about 4000 km,
is still formidable. Prevalent winds at various altitudes help the mi-
grants also over the Caspian Sea and the neighboring deserts, the Middle
East, and the Sahara (Moreau, 1972).
All the circumstances of the journeys mentioned above indicate
that migration to Africa is energetically a very demanding task for small
passerines. There is a wide variety of inhospitable habitats to overcome,
and it is not very well known how birds cope with these conditions.
Our knowledge is also impaired in that what we know about the Pa-
laearctic-African migration system concerns mostly European migrants
crossing the Sahara.
4.5. Recurrence
The faithfulness of birds to breeding grounds is a well-known phe-
nomenon. There is increasing evidence that migrant birds also return
to their wintering grounds in different years. Data on recurrence are
numerous from Africa. Curry-Lindahl (1981) lists 32 species of passer-
ines from 9 African countries from different regions. Yellow Wagtails
had the most retraps (514 from Kenya and 438 from Nigeria; Curry-
Lindahl, 1981), but high recapture rates also were found for the Reed
Warbler (16 of 120 in Uganda) and the Great Reed Warbler (A. arun-
dinaceus) (5 of 13 in Zaire).
Wintering or stopover site fidelity has been demonstrated at various
sites in the Mediterranean (Finlayson, 1980; Herrera and Rodriguez,
1979; L6vei et 01., 1986; Benvenuti and Iolae 1980) (see Table I). Very
few data are available from possible stopover sites in Asia or Africa.
At the Gabes oasis, Tunisia, Winchats (Saxicola rubetra) showed a
recapture rate of 1% (Curry-Lindahl 1981), demonstrating faithfulness
to migratory routes.
Considering the difficulties of obtaining recoveries from wintering
or stopover sites, these results strongly suggest that small passerines
are faithful to their winter quarters or to several winter quarters (see
Section 5.2.1), and perhaps even to migratory stopover sites. This mech-
PALAEARCTIC-AFRICAN PASSERINE MIGRA nON 159
TABLE I
Winter Recurrence of Small Passerines on Mediterranean Wintering Grounds
(%) Recurrence
Species Place 1st year 2nd year Source
Dunnock Central Italy 16.5 57.1 Benvenuti and Ioale (1980)

Southern Italy 10.6 53.7 Liivei and Scebba (unpublished data)
Robin Central Italy 11.6 34.0 Benvenuti and Ioale (1980)
Gibraltar 5.0" Finlayson (1980)
Southern Spain 10.8" Herrera and Rodriguez (1979)
Southern Italy 6.3 30.6 Liivei and Scebba (unpublished data)
Blackcap Gibraltar 9.0" Finlayson (1980)
Southern Spain 5.3" Herrera and Rodriguez (1979)
Chiffchaff Gibraltar 11.0" Finlayson (1980)
Southern Spain 5.1 " Herrera and Rodriguez (1979)
Firecrest Central Italy 11.9 57.1 Benvenuti and Ioale (1980)
"First-/second-year recaptures not distinguished in the original.
anism seems to correspond to Baker's (1978) idea of calculated migra-

tion. Data on recurrence are also numerous from the Neotropics (e.g.,
Gauthreaux, 1982; Kricher and Davis, 1986, and references cited therein).
5. MIGRANTS ON THEIR WINTERING GROUNDS
5.1. Wintering in the Mediterranean

An important consequence of the shape of Eurasia is that the area
under the winter rain sclerophyllous region is much more extensive in
the Old World, due to the influence of the Mediterranean Sea, than in
America, where the Cascades and the Sierra Nevada mountains confine
this region to a narrow strip along the Pacific coast (Walter, 1973). The
Mediterranean region is an important scene of the Palaearctic migration,
both as a stopover site for refueling and resting before and after the
Saharan crossing and as a wintering area for several species of passer-
ines.
In this zone, cyclonic rains occur in winter. The summer is hot
and dry, resulting from a high-pressure zone above the Azores. The
main growing season is spring. Shrubs start to bloom in March, lasting
until June, when a dormant period follows, during the hottest and driest
months. Growth recommences with the autumn rains.
Much of the original vegetation of the Mediterranean region was
160 GABOR L. LOVE!
evergreen sclerophyllous forest with the holm oak Qercus ilex. The
shrub layer was and now is composed of 3- to 5-m-tall bushes; in
favorable places, these may develop into big trees. The shrub layer is
composed of species of Viburnum, Phyllirea, Pistacia, Rhamnus, Rosa,
and lianas Smilax, Lonicera, and Clematis. Only small patches of this
association have remained, because beginning with some of the most
ancient civilizations the natural vegetation has been transformed almost
completely. Where the trees are cut down every 20 years, and on slopes
where the soil is too shallow to support trees, bushes of the height of
a man will develop (called maqui). In places where young woody plants
are cut every 6-8 years and the area is regularly burned or grazed, trees
disappear entirely, and garigue is formed, often dominated by low cush-
ions of the oak Quercus coccifera or juniper Juniperus oxycedrus (Wal-
ter, 1973). In the northern margins of the Mediterranean, there are
humid altitudinal belts in the mountains. The sclerophyllous forest is
succeeded by a deciduous forest belt with oak and chestnut Castanea
sativa, above which beech and fir forests occur (Walter, 1973).
Many woody plants in this region have fleshy fruits, which ripen
during autumn and winter. Fruit-producing species are dominant, either
in amount of cover or in number of species. In southern Spain, fruiting
shrubs and trees cover 56-77% of the surface; 63-77% of the species
bear fruits during autumn and winter (Herrera, 1984a). Many of these
rely on birds for seed dispersal (e.g., Jordana, 1982). Several species
show high lipid content, up to 58% (Herrera, 1984a). Fruit density is
highest between October and January. Fruits that ripen in summer and
autumn have more water and carbohydrate than do fruits of those spe-
cies that ripen during winter, while the lipid content of the fruits in-
creases from summer to winter (Debussche et a1., 1987).
Fruits form the most abundant food resource during autumn and
winter, and most species of transient migrants and wintering birds
consume fruits (Herrera, 1984a; Izhaki and Safriel, 1985; Jordana, 1981,
1985). These include bird species that are insectivorous during the
breeding season (Herrera, 1977, 1981; Jordana and Herrera, 1981; De-
bussche and Isenmann, 1983, 1985a,b). Frugivorous passerines form an
important part of the winter bird communities in Mediterranean areas,
constituting 25-50% of all birds (Jordana, 1985; S. Scebba and M. Mil-
one, unpublished observations; Telleria and Santos, 1986). From sum-
mer to winter, the density of frugivores was found to increase 6- to 15-
fold in the south of Spain (Jordana, 1985); and 8- to 12-fold on a south-
ern Italian island (L6vei et a1., 1985, 1986). Many of the species are
also morphologically adapted to frugivory (Herrera, 1984b; Jordana,
1987).
The timing of fruit ripening and the dependency of migrants on

frugivory have given rise to the hypothesis that there was a coevolu-
tionary relationship between avian dispersers and Mediterranean plants
(Herrera, 1982). In a more detailed study designed to test this hypoth-
esis, Herrera (1987) examined quantitative and qualitative character-
istics of 111 Iberian vertebrate-dispersed plants and the analysis "failed
to reveal an overwhelming influence of the disperser/dispersal envi-
ronment." Of the traits studied, only bicolored displays and seed and
fruit sizes were presumed to have originated from the interaction with
frugivores (Herrera, 1987). This resource is, however, very important
to migrants and winterers. High fruit-removal rates were observed in
Israel (Izhaki and Safriel, 1985), Spain (Herrera, 1984a), and southern
Italy (Lovei, unpublished observations).
Members of the family Turdidae are the most important species
wintering in the Mediterranean, including several sylviid warblers, the
Robin (Erithacus rubecula), the Blackbird (Turdus merula), the Dun-
nock (Prunella modularis), and the Chiffchaff (Phylloscopus collybita)
(Herrera 1984a; S. Scebba and M. Milone, unpublished observations;
Telleria and Santos, 1986). Several of these species show wintering site
fidelity (see Table I) but also a varying degree of nomadism (Finlayson
1981; Debussche and Isenmann, 1984, 1985c; Rodriguez de los Santos
et aI., 1986; Lovei et aI., 1986), which is supposedly in connection with
the abundance of food resources at wintering sites.
Some species establish wintering territories, e.g., the Robin (Pet-
tersson, 1986; Lovei et aI., 1986) and intraspecific aggression has been
observed in the Robin (Lovei, personal observations) and the Blackcap
(Berthold, 1986). Similar behavior has been observed in several species
at New World wintering grounds (Rappole, 1988). The existence of
floater populations was indirectly demonstrated in the Robin in south-
ern Italy (Lovei et al., 1986) and Greece (Petersson, 1986); territory
holders and adult birds were in better condition than were floaters and
first-year birds.
Migrant and wintering birds do not predominate in all Mediter-
ranean habitats. Herrera (1978) found that residents in a southern Span-
ish forest (which, for some species may have included wintering im-
migrants) were more abundant than nonresidents (the latter being no
more than 16% of all birds censused in any month). Nonresidents showed
a wider within-species foraging diversity and used a wider diversity of
foraging tactics. The dominance of residents was attributed to the low
degree of seasonability in food availability (Herrera, 1978). The opposite
was found by Lack (1986b) in an analysis of ecological correlates of an
East African bird community (see Section 5.2).
162 GABOR L. LOVE!
5.2. Resource Use by Migrants in Africa

Resources are highly seasonal in most areas frequented by Pa-
laearctic migrants and resource use follows a complex pattern in space
and time. For example, on the Serengeti plains, migrants arrive 2 months
before the rainy season starts and concentrate at local rainstorms which
attract insects. African birds do not regularly use this resource. After
November, migrants intersperse with residents (Sinclair, 1978).
This complexity is well illustrated by a study in the Tsavo East
National Park in southeast Kenya (Lack, 1983, 1985, 1986a,b, 1987).
The area is an extension of the Somali arid belt and has an average
annual rainfall of 549 mm, with two dry and two wet seasons. The
vegetation ranges from grassland to woodland and is dominated by
bush and wooded grassland, with bushes and trees covering up to 20%
of the surface (Lack, 1985). Twenty species of African visitors plus 19
species of Palaearctic migrants were found. There was a low of one
visitor and no migrant species in June and July and a peak of 11-16
visitor and 16-12 migrant species in December and January. (Visitors
are intra-African migrants; residents are true residents of the Tsavo
area.) More residents were in the thicker habitats and more visiting
species in the open areas. Most (82%) of the species, including all
Palaearctic migrants, were insectivores; 18 of the 20 frugivorous species
were residents.
Granivorous birds dominated (61% of all birds censused) in the
nonwoodland habitat, while more were frugivores (26%) in the wood-
land habitat. Woodland also had a higher proportion of polyphagous
birds (37%) than did any other of the censused habitat types. Bird
densities varied between 4- to 14-fold in different habitats, with peaks
of abundance in the wet season. The peak of granivorous birds was
restricted to 2 months. The insectivore peaks were almost exclusively
due to Palaearctic migrants. In woodland, the frugivores peaked in the
middle of the year, insectivores showed two peaks; the larger one, in
December and January, was again caused by Palaearctic migrants. The
African insectivores (including those eating fruits and arthropods) peaked
in August.
All Palaearctic migrants in this study area ate insects. There was
a very sharp rise in bird abundance in December, then a steady decrease
until April, after which they almost disappeared until November. Twenty
species were common; all but one were passerines. The 11 ground-
feeding species (mainly chats [Lanius] and wheatears [Oceananthe])
arrived in November, and stayed until March. Those feeding in the
woody vegetation (9 species of sylviid warblers) arrived later, near the
PALAEARCTIC-AFRICAN PASSERINE MIC;RATION 163
end of the rains, stayed for about 1 month, disappeared for January and
February, and reappeared in March and April (Lack, 1983).
The difference in the behavior of the ground-feeders and the veg-
etation-feeders at Tsavo can be explained in terms of food availability.
Leaves in Tsavo do not stay on the woody vegetation after mid-January;
consequently, insect abundance is probably reduced substantially until
April rains arrive. During this time, areas farther south are having rains,
so food resources are more favorable there and migrants move on from
Tsavo. The less severe dry season and more rain in the more southerly
areas mean higher grass and herb-layer vegetation. Even if ground-living
arthropods are more abundant. the greater amount of plant cover may
mean less available prey, as most ground-feeders rely on seeing their
prey from a perch or running along open, bare ground (Lack, 1983).
Thus, areas with poorer ground vegetation can be more profitable to
these birds.
On the Serengeti plains, although 81 % of overall food requirements
were satisfied by arthropods, major components of the avifauna did not
track short-term variation in arthropod food resources (Folse, 1982).
Consumption was estimated to be 2°1c, of standing crop/day. Folse (1982)
identified proximate stimuli for habitat selection as vegetation biomass,
height and above-ground vertical structure.
Lack (1986b) also evaluated ecological correlates of the bird assem-
blage at Tsavo. A higher proportion of residents (34%) than visitors
(13%) were food generalists, and these predominantly joined the ground
gleaners when feeding on insects. Specialist frugivores took a wide
selection of fruits. This finding conflicts with Herrera's (1978) argument
that residents are more specialized than are nonresidents. In Tsavo the
lean season is very dry and the wet season is unpredictable and it
therefore may be necessary for a resident to be a generalist in order to
survive at all.
5.2.1. Step Migration

The seasonality of the resources in most places can be an expla-
nation for the fact that many birds do not seem to spend all winter at
the same wintering site. The birds wintering at Tsavo, for example, do
not arrive there before the rains (Lack, 1983). They are believed to spend
time at several sites, performing a step migration. These species leave
the Palaearctic in August and September and cross the Sahara soon
afterward. These regions, at the end of the dry summer, offer little to
migrants. South of the Sahara, the Sahel is at the end of the wet season;
vegetation is lush and insects are very abundant. Migrants do no appear
164 GABOR L. LOVE!
farther south for about 6 weeks and presumably stop in this area, re-
plenishing their fat reserves. This stay in the northern tropics is fol-
lowed by a second major migration farther south. The best evidence
for this stems from ringing work at Ngulia, Tsavo West National Park,
Kenya (Pearson and Backhurst, 1976). Birds are caught at lights, which
indicates that they perform nocturnal migration. Many individuals of
several species have appreciable fat reserves, suggesting that they were
engaged in prolonged flight.
Observations on arrival at and departure from different places in
Africa also suggest that migrant passerines perform a step migration
with several stopover sites, as suggested earlier (Morel, 1968; Moreau,
1972; Dowsett-Lemaire and Dowsett, 1987). The pattern of migratory
restlessness of the Marsh Warbler also corresponds to this pattern (Bert-
hold and Leisler, 1980).
Step migration, on a smaller scale, is found in West Africa too
(Morel, 1968), but involves longer distances than in East Africa. Birds
in the West African savanna concentrate more in riverine forests as the
dry season progresses (Morel and Morel, 1974). Areas with better con-
ditions do not exist within several hundred kilometers. In East Africa,
however, a few hundred kilometers farther south, conditions are much
more favorable.
Such differences between West and East Africa are also found in
spring. Conditions in March and April are very poor in West Africa,
and birds move to areas of local superabundance such as Lake Chad
(Morel and Morel, 1974; Elgood et 01., 1966). In East Africa, the "long"
rains produce fairly good conditions over wide areas, so migrants do
not need to go to special sites in order to accumulate fat reserves prior
to migration.
Many migrants, including those that migrate within Africa, use
resources that are only seasonally available (Lack, 1983). There is a
permanent floating population of birds that breed where they can raise
the most young. For some species this is Tsavo, for others elsewhere
in Africa and for the so-called Palaearctic migrants this is the northern
temperate zone (Lack, 1983). Lack sees no real difference among these
species except the distance they cover during the year.
Palaearctic migrants do not seem to use secondary habitats, as has
been suggested for the Nearctic migrants (see Keast and Morton, 1980).
Their pattern of resource use seems to fit Karr's (1976a) suggestion that
migrants in the Neotropics are using superabundant or sporadically
available resources. Robinson et 01. (1988), studying habitat use of mi-
grants in Amazonia, also indicated that most migrants that winter in
the lowlands, either Nearctic, austral, or intratropical, use resources

that are abundant but only sporadically available.
5.3. Migrants and the Local Avifauna

In his book on Palaearctic-African bird migration, Moreau (1972)
discussed at length the "avian environment," listing the migrant and
native species by families and selected habitats, and evaluating size
relationship as a cue for potential competition. In most cases, species
packing was not dense. However, detailed studies on this subject are
few. Territoriality is often observed in wintering passerines, and re-
peated use of the same territory during the same and in different winters
is also reported for several species (Curry-Lindahl, 1981).
Lack (1985) gave detailed accounts of the habitat preference, feed-
ing method, occurrence, and other factors of the most common species
in his Tsavo studies. The two families richest in migrant species were
the thrushes (Turdidae) and the warblers (Sylviidae). There were 11
regular turdids, 7 of which were Palaearctic migrants. Although there
were similar-sized potential competitors to all four Afrotropical species,
only the Rufous Bush Chat (Cercotrichas galactotes) had a fairly com-
mon resident congener, the White-browed Scrub Robin (C.leucophrys).
Their habitat preferences overlapped and both took its prey from the
ground. However, the Scrub Robin took items mainly from litter and
the Rufous Bush Chat from bare ground and farther from bushes.
Another group of potential competitors is the wheatears (Oen-
anthe). There were three Palaearctic migrants and their Afrotropical
counterpart, the Capped Wheatear, O. pileata. The Capped Wheatear
was rare, which made competition unlikely, but it arrived in Tsavo
mainly after the migrant wheatears left. It is possible that Palaearctic
species delay the arrival of the Capped Wheatear. The three migrant
wheatears, the Pied (0. pleschanka), the Isabelline (0. isabellina) and
the Northern Wheatear, superficially very similar, have different habitat
preferences and different methods of catching prey (Lack, 1985). Leisler
et a1. (1983), however, reported that the three palaearctic wheatears
maintained interspecific territories.
The warblers (Sylviidae) had a total of 30 species in Tsavo, but
only Palaearctic migrants and four Afrotropical species were common.
The two Sylvia species, the Whitethroat and the Barred Warbler (S.
nisoria), had different habitat preferences and were seasonally not over-
lapping. The four Afrotropical species were very different from any
Palaearctic migrants, either by feeding methods or by habitat preference.
166 CABOR L. LOVE!
The Grey Wren Warbler (Camaroptera simplex) was most similar to

the Whitethroat. There was a significant difference in the feeding height
of the two species (Lack, 1985). Lack also noted that the Yellow-breasted
Apalis (Apalis flavida) may have been excluded by the Palaearctic
species, with their feeding methods overlapping. However, the Yellow-
breasted Apalis was rarely seen.
Rabol (1987) studied the competition between wintering Willow
Warblers and the local warblers in Kenya. A shift occurs in foraging
behavior of the Yellow-breasted Apalis at the time the Willow Warblers
arrive, but this too can be interpreted by an explanation not invoking
competition. Birds raising young feed them with food different from
their preferred type, which they collect by different foraging techniques.
Brood raising ends around the time the migrants arrive, and birds can
return to their preferred food and way of foraging.
These data show a general separation in habitat and resource use
and indicate that the Palaearctic migrants are integral parts of the win-
tering habitats. They are using resources that are superabundant and
are not used by resident birds (Lack, 1986b).
Wintering migrants in the Neotropics are also considered to be
integral parts of their wintering habitats (Stiles, 1980). It is assumed,
moreover, that the ranges, abundances, and feeding habitats of the mi-
grants have influenced the resource use pattern of the residents (Cox,
1985). Many Neotropical migrants are, as their Old World counterparts,
insectivores and apply varied ecological strategies, such as maintaining
feeding territories (Rappole and Warner, 1980) or joining mixed flocks
(e.g., Hutto, 1980), or using superabundant or sporadically available
resources (Karr, 1976b; Robinson et al.,in press).
Competition seems to be a prevalent idea invoked in the evolution
and ecology of Neotropical migration (Cox, 1985), although Greenberg
(1986) concluded that "evidence suggesting that competition is im-
portant in shaping winter distributions ... is tentative at best." Com-
petition is not so often mentioned when explaining the complexities
of the Palaearctic-African migration. This is perhaps because the main
wintering grounds (savannas) in Africa are more seasonal and circum-
stances are often more severe than conditions in the Neotropics and
researchers are more impressed by the complex adaptations small pas-
serine migrants show during their journey and wintering. Moreover,
avian environments are also different as Africa has a less rich avifauna.
The major mechanism of resource use by the Palaearctic as well as
other African migrants is to use superabundant but spatially and tem-
porally sporadical resources (Lack, 1986b; Sinclair, 1978).
It is interesting to note that although the potential of predation is
widely acknowledged as a major force in shaping ecological commu-

nities as well as life-history traits of species, little attention has been
given to the potential of predation when seeking explanations to ob-
served migratory patterns.
6. CONCLUSIONS
The present global pattern of seasonal migrations must have been

established during the 15,000-20,000 years since the peak of the last
glaciation (Lamb, 1977). We have evidence that migratory birds possess
a very flexible hereditary mechanism (Berthold, 1988b) that enables
them to react to changes in their environment. They have evolved to
use seasonally available resources in places unsuitable for continuous
use (Myers et al., 1987). However, they also depend on a linked chain
of areas necessary to complete their annual cycles. This same advantage
may turn to their disadvantage if one or the other of these areas becomes
unsuitable for migrants.
Concern must be expressed because this is exactly what seems to
be happening. In the temperate zone, an increasingly tidy agriculture
on an increasingly greater area threatens premigratory fattening sites
of several species through decrease of habitat variability. Fragile Med-
iterranean habitats are being transformed and more often degraded.
Most serious of all is, however, the situation in Africa. The disappear-
ance of the rain forests, especially in West Africa, will have an un-
foreseeable impact on the Palaearctic migrants, as the role of these
forests as wintering habitats is not yet clear.
Many species that winter south of the Sahara have recently suffered
a marked decrease in numbers. In several species, such as the White-
throat (Winstantley et aI., 1974), the Sand Martin (Riparia riparia) (Jones,
1987), the Pied Flycatcher (Ficedula hypoleuca), and the Redstart
(Phoenicurus phoenicurus) (Bruderer and Hirschi, 1984), the decline
is now thought to occur due to the Sahel drought, in part a result of
human activities. A long-term monitoring program in Central Europe
(Berthold et aI., 1986) indicated that among the 15 species showing the
most marked decline, 14 were long-distance migrants that winter in
Africa. It is not exactly known which factors are responsible for the
decline; it can be that, due to increasing desertification, too wide stretches
of desert have to be overcome with insufficient fat reserves, e.g., in the
Yellow Wagtail (Wood, 1982). It is also possible that birds cannot fatten
to the degree necessary to complete their migrations successfully (Bert-
hold, 1988a). Most small passerines are insectivorous and depend OIl
168 GABOR L. LOVE!
insect food in Africa as well. A decrease in woody vegetation, as noted

by Lack (1985), can have a serious negative effect on (among others)
the migrant birds.
These prospects are alarming. Many facets of this complex puzzle
remain to be solved, and it seems that every new development should
at once be applied to help conservation work. Research is preferentially
to be continued on a wider spatial scale, especially on the wintering
grounds. In the end, it may turn out that one of our important resources
will run short: time, to understand and save the Palaearctic-African
bird migration system.
7. SUMMARY
During geological times, both the source and the reception areas
of the Palaearctic-African migrants have undergone enormous climatic
and vegetation changes. The peak of the number of Palaearctic migrant
birds was about 5000 years BP; since then, numbers have decreased
substantially.
Africa as a reception area has a less rich avifauna than the Neo-
tropics; differences in the area of the forest refugia during the Pleis-
tocene or differences in relief complexity are probably responsible.
Most Palaearctic migrants belong to the thrush (Turdidae) and warbler
(Sylviidae) families. Migrants to Africa (unlike those to the Neotropics)
must overcome substantial geographical barriers (deserts and seas); their
migratory behavior is not very well known. Some species make long
continuous flights; others seem to make several shorter ones, even when
crossing the Sahara.
Bird densities show considerable seasonal fluctuations although
much less than in the Neotropics. Most migrants winter north of the
equator; the savannas are the most important wintering habitats. The
importance of the rain forests as wintering habitats is not known but
is probably not insignificant.
The Mediterranean Basin is an important stopover-wintering area
for several species. Energy-rich, highly nutritious fruits are available
during the Mediterranean winter, and most wintering species feed on
them.
Resource fluctuations in Africa are governed by rainfall regimes
and typically show a 6- to 15-fold difference between the dry and the
wet seasons, with even more on the West African savannas. Conditions
are good at the time the migrants arrive and deteriorate during their
wintering period.
PALAEARCTIC-AFRICAN PASSERINE MIGRATION H,9
Most migrants to Africa are insectivorous and use abundant but

sporadically available resources. They perform a step migration, spend-
ing time at several wintering areas in a defined sequence. Most species
of migrants and residents segregate in resource use; competition is not
demonstrated. Residents are more generalists than winterers, probably
because of the scarcity of the resources during the lean season.
Several long-distance migrants showed a marked decrease in the
last 15 years. Their conservation requires coordinated action on a wide
spatial scale.
ACKNOWLEDGMENTS. I would like to thank Dr. D. L. Pearson for dis-

cussion; Drs. P. Berthold, H. Biebach, T. Csorg6, P. C. Lack, D. Pomeroy,
J. Rabol, S. K. Robinson, and S. Scebba, for providing unpublished
information and manuscripts; Drs. G. Backhurst, P. Jordano, and T.
Szekely, for kind help with literature otherwise unavailable to me; and
Mrs. J. P. Fazekas, for her help in preparing the manuscript. I am grateful
to Dr. D. M. Power for linguistic corrections. This is publication no. 9
of the Passerine Migration and Wintering Research Group, Hungarian
Ornithological Society.
REFERENCES
Bairlein. F .. 1985a. Efficiency of food utilization during fat deposition in the long-distance
migratory garden warbler. Sylvia borin. Oecologia 68:118-125.
Bairlein, F .. 1985b, Body weight and fat deposition of Palaearctic passerine migrants.
Oecologia 66:141-146.
Bairlein. F .. 1987, The migratory strategy of the Garden Warbler: A survey of field and
laboratory data. Ring. Migr. 8:59-72.
Bairlein. F., Beck. P., Feiler. W., and Querner, U., 1983. Autumn weights of some Pa-
laearctic passerine migrants in the Sahara. Ibis 125:404-407.
Baker. R. R.. 1978. The Evolutionary Ecology of Animal Migration. Hodder and Stouton.
London.
Benvenuti, S., and loale, P., 1980. Fedelta al luogo di svernamento, in anni successivi.
in alcune species di uccelli. Avocetta 4:133-139.
Berthold. P .. 1985, Physiology and genetics of avian migration, in: Migration: Mechanisms
and Adaptive Significance (M. A. Rankin, ed.). Contr. Marine Sci., Supp!. 27, pp.
526-543.
Berthold, P .. 1986. Wintering in a partially migratory Mediterranean Blackcap (Sylvia
atricapilla) population: Strategy, control, and unanswered questions, Ric. Biol. Sel-
vaggina (supp!.) 10:33-45.
Berthold. P .. 1988a. The biology of the genus Sylvia-a model and challenge for Afro-
European cooperation. Tauraco 1. (in press).
Berthold. P., 1988b. The control of migration in European warblers, Proc. XIX. Int. Or-
nithol. Congr. (in press).
170 CABOR L. LOVE!
Berthold, P., and Leisler, B., 1980, Migratory restlessness of the marsh warbler Acro-
cephalus palustris. A reflection of its unusual migration, Naturwissenschaften
67:472.
Berthold, P., and Querner, U., 1981, Genetic basis of migratory behavior in European
warblers, Science 212:77-79.
Berthold, P., and Querner, U., 1982a, Genetic basis of moult, wing length, and body
weight in a migratory bird species, Sylvia atricapilla, Experientia 38:801-802.
Berthold, P., and Querner, U., 1982b, Partial migration in birds: Experimental proof of
polymorphism as a controlling system, Experientia 38:805.
Berthold, P., Fliege, G., Querner, U., and Winkler, H., 1986, Die Bestandsentwicklung
von Kleinvogel in Mitteleuropa: Analyse von Fangzahlen, J. OrnithoI. 127:397-437.
Bibby, C. J., and Green, R. E., 1980, Foraging behaviour of migrant Pied Flycatchers,
Ficedula hypoleuca, on temporary territories, J. Anim. EcoI. 49:507-521.
Bibby, C. J., and Green, R. E., 1981, Autumn migration strategies of Reed and Sedge
Warblers, Ornis Scand. 12:1-12.
Bibby, C. J., and Green, R. E., 1983, Food and fattening of migrating Warblers in some
French marshlands, Ring. Migr. 4:175-184.
Biebach, H., 1985, Sahara stopover in migratory flycatchers: Fat and food affect the time
program, Experientia 41:695-697.
Biebach, H., 1988, Ecophysiology of resting Willow Warblers (Phylloscopus trochilus)
crossing the Sahara, Proc. XIX Int. OrnithoI. Congr. (in press).
Biebach, H., Friedrich, W., and Heine, G., 1986, Interaction of bodymass, fat, foraging
and stopover period in trans-Sahara migrating passerine birds, Oecologia 69:370-379.
Blem, C. R., 1980, The energetics of migration, in: Animal Migration, Orientation, and
Navigation (S. A. Gauthreaux, Jr., ed.), Academic, New York, pp. 175-224.
Brown, L. H., Urban, E. K., and Newman, K., 1982, The Birds of Africa Vol. 1., Academic,
London.
Bruderer, B., and Hirschi, W., 1984, Langfristige Bestandsentwicklung von Gartenroetel
Phoenicurus phoenicurus und Trauerschnaepper Ficedula hypoleuca nach schweiz-
erischen Beringungszahlen und NisthoehlenkontroIIen, OrnithoI. Beob. 81:285-302.
Buskirk, R. E., and Buskirk, W. H., 1976, Changes in arthropod abundance in a highland
Costa Rican forest, Am. MidI. Nat. 95:288-298.
Cox, G. W., 1985, The evolution of avian migration systems between temperate and
tropical regions of the New World, Am. Nat. 126:451-474.
Csorg6, T., and Lovei, G. 1., 1988, Premigratory fattening of the Thrush Nightingale,
Luscinia luscinia, at a stopover site in central Hungary Proc. 2nd Conf. Hung. Or-
nithol. Soc. (in Hungarian) (in press).
Curry-Lindahl, K., 1981, Bird Migration in Africa, Vols. 1-2, Academic, New York.
Debussche, M., and Isenmann, P., 1983, La consommation des fruits chez quelques fau-
vettes mediterraneennes (Sylvia melanocephala, S. cantillans, S. hortensis, S. un-
data) daus la region de Montpellier (France), Alauda 51:302-308.
Debussche, M., and Isenmann, P., 1984, Origine et nomadisme des Fauvettes 11 tete noire
(Sylvia atricapilla) hivernant en zone mediterraneenne fram;aise. L'Oiseau RFO
54:101-107.
Debussche, M., and Isenmann, P., 1985a, An example of Redwing diet in a Mediterranean
wintering area, Bird Study 32:152-153.
Debussche, M., and Isenmann, P., 1985b, Le regime alimentaire de la Grive musicienne
(Turdus philomelos) en automne et en hiver dans les garrigues de Montpellier (France
mediterraneenne) et ses relations avec l'ornithochorie, Terre Vie 40:379-388.
Debussche. M .. and Isenmann. P .. 1985c. Frugivory of transient and wintering European

Robins Erithacus rubecula in a Mediterranean region and its relationship with or-
nithochory. Holarc. Ecol. 8:157-163.
Debussche. M .• Cortez. J.. and Rimbault. I.. 1987. Variation in fleshy fruit composition
in the Mediterranean region: The importance of ripening season. life-form, fruit type
and geographical distribution, Oikos 49:244-252.
Dowsett, R. J.. and Fry. C. H .. 1971, Weight losses of trans-Saharan migrants. Jbis
113:531-533.
Dowsett-Lemaire, F.. and Dowsett. R. J., 1987, European Reed and Marsh Warblers in
Africa: Migration patterns. moult and habitat, Ostrich 58:65-85.
Elgood, J. H .. Sharland. R. E.. and Ward. P.. 1966. Palaearctic migrants in Nigeria. Ibis
108:84-116.
Emlen. J. T .. 1980. Interaction of migrant and resident land birds in Florida and Bahama
pinelands, in: Migrant Birds in the Neotropics: Ecology. Behavior. Distribution. and
Conservation (A. Keast and E. S. Morton. eds.), Smithsonian Institute Press. Wash-
ington D. C.. pp. 133-143.
Finlayson. J. C.. 1980. The recurrence in winter quarters at Gibraltar of some scrub
passerines. Ring. Migr. 3:32-34.
Finlayson. J. C., 1981. Seasonal distribution. weights and fat of passerine migrants at
Gibraltar. Ibis 123:88-96.
Folse. L. J.. 1982, An analysis of avifauna-resource relationship on the Serengeti plains.
Ecol. Monog. 52:111-127.
Fry. C. II .. Ash, J. S .. and Ferguson-Lees. I. J.. 1968. Spring weights of some Palaearctic
migrants at Lake Chad. Ibis 112:58-82.
Gauthreaux, S. A .. Jr .. 1980. The influences of long-term and short-term climatic changes
on the dispersal and migration of organisms. in: Animal Migration, Orientation. and
Navigation (S. A. Gauthreanx. Jr .. ed.), Academic. New York. pp. 103-173.
Gauthreaux. S. A.• Jr.. 1982. The ecology and evolution of avian migration systems. in:
Avian Biology. Vol. 6 (D. S. Farner and J. R. King. eds.). Academic. New York. pp.
93-168.
Gladkov. N. H .. 1957. Birds of the Mangyshlak Peninsula (Caspian). Ibis 99:269-274.
Greenberg. R.. 1986. Competition in migrant birds in the nonbreeding season. Current
Ornithol. 3:281-307.
Gwinner, E.. 1968. Artspezifische Muster der Zugunruhe bei Laubsangern und ihre
mogliche Bedeutung fur Beendigung des Zugs im Winterquartier. Z. Tierpsychol.
25:843-853.
Gwinner. E.. 1977. Circannual rhythms in bird migration. Annu. Rev. Eco!. Syst.
8:381-405.
Gwinner. E., and Wiltschko, W., 1980. Circannual changes in migratory orientation of
the Garden Warbler, Sylvia borin. Behav. Ecol. Sociobiol. 7:73-78.
Herrera. C. M., 1977, Ecologia alimenticia del Pettirrojo (Erithacus rubecula) durante su
invernada en encinares del Sur de Espana. Donana Acta Verteb. 4:35-59.
Herrera, C. M .. 1978, Ecological correlates of residence and non-residence in a Mediter-
ranean passerine bird community. J. Anim. Ecol. 47:871-890.
Herrera, C. M., 1981. Fruit food of Robins wintering in southern Spanish Mediterranean
scrubland. Bird Study 28:115-122.
Herrera. C. M .• 1982. Seasonal variation in the quality of fruits and diffuse coevolution
between plants and dispersers. Ecology 63:773-785.
172 GABOR L. LOVE!
Herrera, C. M., 1984a, A study of avian frugivores, bird-dispersed plants, and their in-
teraction in Mediterranean scrublands, Ecol. Monog. 54:1-23.
Herrera, C. M., 1984b, Adaptation to frugivory of Mediterranean avian seed dispersers,
Ecology 65:609-617.
Herrera, C. M., 1987, Vertebrate-dispersed plants of the Iberian peninsula; A study of
fruit characteristics, Ecol. Monog. 57:305-331.
Herrera, C. M., and Rodriguez, M., 1979, Year-to-year site constancy among three pas-
serine species wintering at a southern Spanish locality, Ring. Migr. 2:160.
Hutto, R L., 1980, Winter habitat distribution of migratory land birds in Western Mexico,
with special reference to small foliage gleaning insectivores, in: Migrant Birds in the
Neotropics: Ecology, Behavior, Distribution, and Conservation (A. Keast and E. S.
Morton, eds.), Smithsonian Institute Press, Washington D. C., pp. 181-203.
Izhaki. I., and Safriel, U. N., 1985, Why do fleshy-fruit plants of the Mediterranean scrub
intercept fall-but not spring-passage of seed-dispersing migratory birds? Oecol-
ogia 67:40-43.
Janzen, D. H., 1973, Sweep samples of tropical foliage insects: Effects of seasons, vege-
tation types, elevation, time of day, and insularity, Ecology 54:687-708.
Janzen, D. H., and Schoener, T. W., 1968, Differences in insect abundance and diversity
between wetter and drier sites during a tropical dry season, Ecology 49:96-110.
Jones, G., 1987, Selection against large size in the sand martin Riparia riparia during a
dramatic population crash, Ibis 129:274-280.
Jones, P. J., 1985, The migration strategies of Palaearctic passerines in West Africa, in:
Migratory Birds: Problems and Prospects in Africa (A. MacDonald and P. Goriup,
eds.), Report of the Fourteenth Conference European Continental Section ICBP, 1983,
pp.9-21.
Jordano, P., 1981, Alimentacion y relaciones trolicas entre los passeriformes en paso
otonal por una localidad de Andalucia central, Donana Acta Vert. 8:103-124.
Jordano, P., 1982, Migrant birds are the main seed dispersers of blackberries in southern
Spain, Oikos 38:183-193.
Jordano, P., 1985, El cicio anual de los paseriformes frugivoros en el matorral mediter-
raneo del sur de Espana: importancia de su invernada y variaciones interanuales,
Ardeola 32:69-94.
Jordano, P., 1987, Frugivory, external morphology and digestive system in Mediterranean
sylviid warblers Sylvia spp., Ibis 129:175-189.
Jordano, P., and Herrera, C. M., 1981, The frugivorous diet of Blackcap populations Sylvia
atricapilla wintering in southern Spain, Ibis 123:502-507.
Karr, J. R., 1976a, Within and between-habitat avian diversity in African and Neotropical
lowland habitats, Ecol. Monogr. 46:457-481.
Karr, J. R, 1976b, On the relative abundance of migrants form the North Temperate Zone
in tropical habitats, Wilson Bull. 88:433-458.
Karr, J. R, 1980, Patterns in the migration system between the north temperate zone and
the tropics, in: Migrant Birds in the Neotropics; Ecology, Behavior, Distribution, and
Conservation (A. Keast and E. S. Morton, eds.), Smithsonian Institute Press, Wash-
ington D. C., pp. 529-543.
Keast, A., 1980, Synthesis: Ecological basis and evolution of the Nearctic-Neotropical
bird migration system, in: Migrant Birds in the Neotropics: Ecology, Behavior, Dis-
tribution, and Conservation (A. Keast and E. S. Morton, eds.), Smithsonian Institute
Press, Washington D. C., pp. 558-576.
Keast, A., and Morton, E. S. (eds.), 1980, Migrant Birds in the Neotropics: Ecology,
PALAEARcnC-AFRICAN PASSERINE MIGRATION 173
Behavior, Distribution, and Conservation, Smithsonian Institute Press, Washington

D. C.
Klein, H., Berthold, P., and Gwinner, E., 1973, Der Zug europaischer Garten- und M6nchs-
grasmiicken (Sylvia borin und S. atricapilla), Vogelwarte 27:73-134.
Kricher,). C., and Davis, W. E., 1986, Returns and winter-site fidelity of North American
migrants banded in Belize, Central America, J. Field Ornitho1. 57:48-52.
Kukla, G. )., 1977, Pleistocene land-sea correlations. 1. Europe, Earth Sci. Rev. 13:307-:~74.
Lack, P. c., 1983, The movements of Palaearctic landbird migrants in Tsavo East National
Park, Kenya, 1. Anim. Eco1. 52:513-524.
Lack, P. c., 1985, The ecology of the land-birds of Tsavo East National Park, Kenya,
Scopus 9:2-23, 57-96.
Lack, P. C., 1986a, Diurnal and seasonal variation in biomass of arthropods in Tsavo
West National Park, Kenya, Afr. J. Eco1. 24:47-51.
Lack, P. c., 1986b, Ecological correlates of migrants and residents in a tropical African
savanna, Ardea 74:111-119.
Lack, P. C., 1987, The structure and seasonal dynamics of the bird community in Tsavo
East National Park, Kenya, Ostrich 58:9-23.
Lamb, H. H., 1977, Climate: Present, Past and Future, Vo!' 2, Methuen, London.
Leisler, B., Heine, G., and Siebenrock, K.-H., 1983, Einnischung und interspezifische
Territorialitaet ueberwinternder Steinschmaetzer (Oenanthe isabellina, O. oenanthe,
O. pleschanka) in Kenia, J. Ornitho1. 124:393-413.
Lima, S. L., 1986, Predation risk and unpredictable feeding conditions: Determinants of
body mass in birds, Ecology 67:377-385.
L6vei, G. L., Scebba, S., and Milone, M., 1985, Migration and wintering of the Blackcap
Sylvia atricapilla on a Mediterranean island, Ring. Migr. 6:39-44.
L6vei, G. L., Scebba, S., Minichiello, F., and Milone, M., 1986, Seasonal activity, wing
shape, weights and fat reserve variation of Robins (Erithacus rubecula) in southern
Italy, Ric. Bio1. Selvaggina (Supp!.) 10:229-241.
Meier, A. H., and Fivizzani, A. )., 1980, Physiology of migration, in: Animal Migration,
Orientation, and Navigation (S. A. Gauthreaux, Jr., ed.), Academic, New York, pp.
225-282.
Moreau, R. E., 1972, The Palaeartic-African Bird Migration System, Academic, London.
Morel, G., 1968, Contribution a la synecologie des oiseaux du Sahel senegalais, Mem.
ORSTOM 29:pp.1-179.
Morel, G., and Morel, M.-Y., 1974, Recherches ecologiques sur une savane sahelienne
du Feria septentrional, Senegal. II. Influence de la secheresse de I'annee 1972/73 sur
I'avifaune, Terre Vie 28:95-123.
Myers, j. P., Morrison, R. I. G., Antas, P. Z., Harrington, B. A., Lovejoy, T. E., Sallaberry,
M., Senner, S. E., and Tarak, A., 1987, Conservation strategy for migratory species,
Am. Sci. 75:19-26.
Pearson, D. )., and Backhurst, G. C., 1976, The southward migration of Palaearctic birds
over Ngulia, Kenya, Ibis 118:78-105.
Pearson, D. L., 1975, The relation of foliage complexity to ecological diversity of three
Amazonian bird communities, Condor 77:453-466.
Pearson, D. L., 1982, Historical factors and bird species richness, in: Biological Diver-
sification in the Tropics, (G. T. Prance, ed.), Columbia University Press, New York,
pp. 441-452.
Pennycuick, C. J., 1975, Mechanics of flight, in: Avian Biology, Vol. 5 (D. S. Farner and
j. R. King, eds.), Academic, New York, pp. 1-75.
174 CABOR L. LOVE!
Pettersson, J., 1986, Weight and fat levels in Robins (Erithacus rubecu1a) wintering in
northern Greece, Ric. Biol. Se1vaggina (Supp!.) 10:265-273.
Pomeroy, D. E., 1988, Land bird populations in East Africa, Afr. J. Ecol. (in press).
Pomeroy, D., and Lewis, A., 1987, Bird species richness in tropical Africa: Some com-
parisons, Biol. Conserv. 40:11-28.
Rabol, F., 1987, Coexistence and competition between over wintering Willow Warblers
Phylloscopus trochi1us and local warblers at Lake Naivasha, Kenya, Ornis Scand.
18:101-121.
Rappole, J. H., and Warner, D. W., 1980, Ecological aspects of migrant bird behavior in
Veracruz, Mexico, in: Migrant Birds in the Neotropics: Ecology, Behavior, Distri-
bution, and Conservation (A. Keast and E. S. Morton, eds.), Smithsonian Institute
Press, Washington D. C. pp. 353-393.
Rappole, J. H., 1988, Intra- and intersexual competition in migratory passerine birds
during the non-breeding season, Proc. XIX. Int. Ornithol. Congo (in press).
Raven, P. H., 1976, Ethics and attitudes, in: Conservation of Threatened Plants (J. B.
Simmons, P. E. Brandham, G. 1. I. Lucas, and V. T. H. Parry, eds.), Plenum, New
York, pp. 154-179.
Robinson, S. K., Terborgh, J. W., and Fitzpatrick, J. W., 1988, Habitat selection and relative
abundance of migrants in southeastern Peru, Proc. XIX. Int. Ornithol. Congo (in press).
Rodriguez de los Santos, M., Cuadrado, M., and Arjona, S., 1986, Variation in the abun-
dance of Blackcaps (Sylvia atricapilla) wintering in an Olive (Olea europea) orchard
in southern Spain, Bird Study 33:81-86.
Scebba, S., U:ivei, G., and Caracciolo, A., 1985, Changes in weights and fat reserves of
the Garden Warbler, Sylvia borin and Icterine Warbler, Hippo1ais icterina, during
migration on a Mediterranean island, Proc. 3rd Conf. Ita1. Ornithol. (in Italian) pp.
107-110.
Schilz, E., 1971, Grundriss der Voge1zugskunde, Parey Verlag, Berlin.
Sinclair, A. R. E., 1978, Factors affecting the food supply and breeding season of resident
birds and movements of Palaearctic migrants in a tropical African savannah, Ibis
120:480-497.
Southwood, T. R. E., 1977, Habitat, the templet for ecological stategies?, J. Anim. Ecol.
46:337-365.
Stiles, F. G., 1980, Evolutionary implications of habitat relations between permanent and
winter resident landbirds in Costa Rica, in: Migrant Birds in the Neotropics: Ecology,
Behavior, Distribution, and Conservation (A. Keast and E. S. Morton, eds.), Smith-
sonian Inst. Press, Washington D. c., pp. 421-435.
Telleria, J. 1., and Santos, T., 1986, Bird wintering in Spain. A review, Ric. Biol. Se1-
vaggina (Supp!.) 10:319-338.
Terborgh, J. W., 1980, The conservation status of neotropical migrants: present and future,
in: Migrant Birds in the Neotropics: Ecology, Behavior, Distribution, and Conser-
vation (A. Keast and E. S. Morton, eds.), Smithsonian Institute Press, Washington
D. C., pp. 21-30.
Walter, H., 1973, Vegetation of the Earth, 2nd ed., Springer-Verlag, Berlin.
Welty, c., 1980, The geography of birds, in: Birds (B. Wilson, ed.), W. A. Freeman, San
Francisco, pp. 14-22.
Winstantley, D., Spencer, R., and Williamson, K., 1974, Where have all the Whitethroats
gone?, Bird Study 21:1-14.
Wood, B., 1982, Trans-Saharan spring migration of Yellow Wagtails (Motacilla flava), J.
Zool. 197:267-283.
Zink, G., 1973-1985, Der Zug europaischer Singviige1, Vo!s. 1-4, Vogelzug-Verlag, Miig-
gingen.
CHAPTER 5
BIOLOGY AND CONSERVATION OF

THE CALIFORNIA CONDOR
NOEL F. R. SNYDER and HELEN A. SNYDER
1. INTRODUCTION
On Easter Sunday of 1987, the last California Condor (Gymnogyps cal-

ifornianus) known to exist in the wild was trapped for captive breeding,
joining 26 others of his species at the San Diego and Los Angeles Zoos.
A young male adult, he was a bird whose life had been followed closely
for a number of years. His movements and interactions with other con-
dors, his molting patterns and changes in coloration with age, as well
as his pairing with an old female in late 1985, and his first breeding
attempts in 1986 had all been documented in considerable detail. Like
every other bird in the remnant population, he was known and had
been studied as an individual. With his capture, an era of intensive
investigations of condor natural history and ecology had corne to a
close.
The trapping of the last wild condor was perceived in a variety of
ways. For some, this was the final catastrophe in a fundamentally flawed
and wasteful effort to save the species, an effort based on misguided
technology rather than on respect for the species' needs for space and
solitude. For these people, the condor was preeminently a bird that
should be left alone, a creature of wilderness that was inseparable from
its habitat and had to be protected by isolating it as much as possible
from interactions with man. They believed the condor was so extremely
sensitive to disturbance that it could not even be studied closely with-
NOEL F. R. SNYDER and HELEN A. SNYDER • Portal, Arizona 85632.

175
176 NOEL F. R. SNYDER and HELEN A. SNYDER
out irreparable harm. And it did not need to be studied. Its problems
were long ago determined by Carl Koford and the McMillan brothers
to be shooting, 1080 poisoning, and disturbance. That the road to sal-
vation of the condor lay in countering these threats and in habitat
preservation was beyond dispute, and that these needs still remained
largely unaddressed was a sad commentary on the unresponsiveness
of bureaucracy to conservation priorities. Furthermore, the sanctity of
the California Condor had been tragically defiled by callous manipu-
lative procedures such as radiotelemetry and now by incarceration of
the last individuals. The loss of the species was an accomplished fact;
the individuals taken captive and deprived of their natural surround-
ings were no longer condors.
For others, the trapping of the last wild condor, although a pro-
foundly sobering event, was by no means the end of efforts to save the
species. It was instead an important and fundamentally positive step
toward ensuring the viability of a captive population that would some-
day serve as a source for reestablishing self-sustaining wild populations
in various portions of the species' former range. For these people, recent
successes with programs to reintroduce other large birds to the wild
from captivity offered great hope that the same could be accomplished
with condors. They were convinced that the loss of the last population
of wild condors was unavoidable because of insuperable difficulties in
maintaining the species in its last range. They were convinced as well
that if the last birds were not taken captive, the long-term chances for
re-establishing the species in more favorable locations in the wild would
be greatly diminished.
While the above contrasting viewpoints are representative of the
perceptions of a significant fraction of the people involved with condor
conservation in recent years, they are far from the only viewpoints that
have been held. For if there is one thing certain in this world, it is that
no two people think exactly alike on the subject of efforts to save the
California Condor. The process of attempting to preserve this species
has been as much a political as a biological endeavor and has involved
endless polemics, confrontations, and debates, as well as endlessly
shifting alliances, as old controversies have been resolved and new
issues have arisen.
The condor arouses strong human emotions and has represented
many different values for different people. For these reasons, it is a
very difficult task to evaluate fairly the history of efforts to save it,
perhaps especially so for those, such as ourselves, who have been par-
ticipants in the struggles. What is truth and objectivity for one person
is prejudice and propaganda for another, and it is unlikely that any
single account of the species might satisfy everyone.
CONDOR BIOLOGY AND CONSERVATION 177
But pleasing everyone is not our goal. What we hope to achieve

here is something rather different-a fulfillment of what we take to be
an obligation to provide as perceptive and candid an evaluation of the
conservation program as we are able to prepare. The public has paid
large sums of money for this program and has been greatly concerned
about its success. As a consequence, the public is entitled to know, not
just from professional journalists and bureaucrats, but from the people
actually doing the work at the field level, how effectively the major
goals of the program have been met and how practical various alter-
native conservation strategies for the future really are. As field biologists
in the program from 1980 to 1986, primarily involved with reproductive
studies, censusing efforts, and the efforts to establish a captive popu-
lation, we believe we have an obligation to make such an assessment,
especially since the recent picture of condor conservation that has
emerged in the popular and scientific press has been so distressingly
superficial.
In this account, we attempt to sort out significant events in the
history of biological studies and conservation efforts as objectively as
we can. We hope that what we present will be judged on its own
intrinsic merits and accuracy, rather than by how well it conforms to
conventional conceptions of the species. We hope as well that it will
become clear that no one who has participated in the efforts to save
the species or sat on the sidelines has ever had perfect foresight, and
that the process of conservation of the species has necessarily been an
evolving discipline, crucially dependent on continuing research to im-
prove understanding of the nature of the species' problems.
Many mistakes have been made indeed, and these mistakes need
to be analyzed and thoroughly understood if they are not to occur again.
Yet, at the same time much that is positive has also occurred, a sur-
prising amount, in fact. We believe it is worth examining the record
closely, both the positive and negative aspects, for what can be learned
as to how well the conservation and research processes have taken
place and how they might be improved. The condor is not the last
endangered species that will be driven to the wall, and a thoughtful
review of these matters may help avoid problems for other efforts in
the future.
2. HISTORY OF BIOLOGICAL STUDIES
The California Condor has been a subject of intense interest among

naturalists for well over a century and a focus of conservation and
research efforts for nearly a half century. Foremost among early re-
searchers was Carl Koford, whose monumental pioneering monograph

(Koford, 1953) covered field studies conducted during the late 1930s
and 1940s. Koford's studies were supported by the University of Cal-
ifornia at Berkeley and the National Audubon Society (NAS) and formed
the basis for his Ph.D. dissertation. Other well-known NAS-supported
condor researchers were two rancher-naturalists, the McMillan brothers
(Ian and Eben) who, together with Alden Miller, published a follow-
up monograph to Koford's original studies (Miller et 01., 1965) and a
very readable popular account of the species (McMillan, 1968). Less
well known for his contributions, as he never published a condor mono-
graph, but no less admirable for the quality of his efforts, was Fred
Sibley, who was the first U.S. Fish and Wildlife Service (USFWS) con-
dor biologist from 1966 to 1969. Sibley was followed by Sanford Wilbur,
who led the USFWS condor program from 1969 through the stormy
transition period to the start of an intensive final effort in early 1980.
Wilbur also published a monograph on the species (Wilbur, 1978), as
well as a number of other shorter papers on aspects of its biology.
These were not the only researchers to have worked intensively
with the species over the years, but they were the most prominent
individuals of their times, and thus it is convenient, if not totally fair,
to divide the history of biological studies prior to the modern program
into eras bearing their names.
2.1. The Pre-Koford Era

Prior to Koford's study, one of the principal sources of information
on condors was data gathered by egg collectors. With the well-known
rarity of the condor, its eggs were extremely valuable, and this provided
a strong incentive for individuals to seek out the species. Egg collecting
reached a peak around the turn of the present century, and altogether
over 70 eggs were taken by the 1940s (Kiff, 1983). However, the sorts
of information obtained by the egg collectors were limited-egg dates,
nest site characteristics, breeding range, and some unsystematic data
on natural history.
The early collectors, such as Kelly Truesdale, so marvellously de-
scribed by Ian McMillan (1968), either did not know about multiple
clutching in the species or they were not letting on (any publicity here
would have had the effect of enabling competitors to collect more eggs,
thus reducing their value). Very likely, they simply did not know. In
recent years, we have been able to document that condors routinely
move distances of several kilometers to lay replacements (Snyder and
Hamber, 1985), and unless one is able to identify individuals and to
CONDOR IlJOLOCY AND CONSERVr\TION 17q
follow them closely over some formidably rugged terrain, it is unlikely

that one would become aware of this capacity of the species. Most
collectors knew of only one or two nesting sites and checked these each
year, noting that the species used these sites only irregularly, never
laid more than a single egg, and never laid replacement eggs (at least
in the sites they knew about). An excellent summary of the egg collector
data is given in Koford (1953).
Aside from the egg collectors, there was considerable interest in
the species from early bird photographers and naturalists. In 1906, two
of these individuals, W. L. Finley and H. T. Bohlman, carried out a
periodic study of a nesting pair in the San Gabriel Mountains north of
Pasadena, and made what are unquestionably the most significant early
observations of the behavior and natural history of the species, illus-
trated by a set of remarkably fine photographs. In a series of papers and
articles, Finley (1906, 1908a-d, 1909, 1910) and Finley and Finley
(1915, 1928) described this study in detail and also presented an ex-
cellent summary of the state of knowledge of the species' status and
decline.
Finley's perception of the condor was not that it was a species
incredibly wary of man but that it was a very approachable bird at the
nest and was a species suffering greatly from shooting and from poi-
soning, especially that practiced to rid the mountains of southern Cal-
ifornia of grizzly bears (Ursus horribilis). Though later workers (e.g.,
Koford. the McMiIlans) came to project an image of the species as one
behaviorally intolerant of human disturbance around nests, and Harris
(1941). Koford (1953), and Wilbur (1978) questioned the impacts of
early poisoning campaigns. our own perceptions of the species' ap-
proachability and early difficulties closely parallel those of Finley. To
our knowledge, there is simply no evidence that human disturbance
short of nest robbing or destruction of eggs or chicks has ever caused
the desertion of an active condor nest. And some nests have been sub-
jected to impressive amounts of disturbance, including the one studied
by Finley and several of the sites studied by Koford (1953). In fact,
there are many records of persistent return of pairs to certain sites
despite repeated robbing of eggs and young (although replacement eggs
within seasons have almost always been laid in alternative sites).
The reluctance of Harris (1941), Koford (1953), and Wilbur (1978)
to accept the many published reports that condors in the 19th century
were being heavily stressed by predator-poisoning campaigns (primar-
ily using strychnine) rests on the fact that these accounts were largely
hearsay and not backed up with detailed substantiation or eyewitness
information. However, hearsay reports are not always inaccurate, and
the finding of apparent strychnine-poisoned condors during the 1950s

and 1960s (Borneman, 1966; McMillan, 1968) gives evidence of sen-
sitivity of the species to this toxicant. That there was massive poisoning
of large predators with strychnine-laced carcasses during the 1800's is
not in question, and it would be surprising if condors were not suffering
as a result.
In this connection, it is informative to repeat an account by Jose
Jesus Lopez, the venerable foreman of the Tej6n Ranch, as presented
by Frank Latta, in his fascinating Saga of EI Rancho Tej6n (1976). This
account leaves little doubt as to the devastating impacts of early poi-
soning practices on condors, especially when considered in conjunc-
tion with the accounts of Finley and others:
For a number of years before I arrived at the ranch [1874], Mr. Beale had
employed Pete Miller to kill bears. This he did by shooting, trapping, and
poisoning. In the mountains he hunted them, and also caught them in traps
or deadfalls made of heavy timbers. When they killed sheep or cattle he put
poison in the carcasses. Strychnine generally was used in such poisoning,
but Miller used a special poison of his own. The nature of this poison he
kept secret from everyone. It would kill everything; condors, buzzards, crows,
ravens, foxes, coyotes, wolves, coons, wild cats, mountain lions, and bears.
We even had dogs, valuable dogs, killed by this poison. Later I learned that
Miller used cyanide of potassium. I was assured by everyone that before
this poisoning was done, both wolves and condors were plentiful in the
Tej6n country.
With the benefit of knowledge obtained since 1980 we would add

one more early stress to the two given by Finley-lead poisoning, an
indirect and inadvertent consequence of the shooting of other animals
and subsequent ingestion by the condors of carcasses contaminated
with lead bullet fragments. In fact, it is reasonable to suppose that the
historical decline of the condor began with a vengeance, once the twin
stresses of shooting and lead poisoning were introduced with the arrival
of European man.
There is no good evidence that the downward population trend of
the wild condor population has ever been reversed for any period since
the species was first described. Koford (1953) and McMillan (1968)
argued for historical periods of increase or relative stability of the pop-
ulation primarily on the basis of condors moving into certain local
foraging regions where they had not been seen earlier and on the basis
of ephemeral local increases in the sizes of flocks reported in portions
of the foraging range. However, continual minor changes in foraging
range and fluctuations in local numbers in foraging areas occur as a
natural consequence of shifts in food distribution and density, regard-
less of whether the population as a whole is increasing or decreasing.
CONDOR BIOLOGY AND CONSERV ArION IHI
A careful inspection of the historical distributional data gathered by

Koford (1953) suggests an overall steady contraction in range and num-
bers.
Besides Finley, there is one other individual who deserves special
mention in the pre-Koford years, though his important role in early
condor studies has received virtually no recognition. This was Cyril S.
Robinson of the U. S. Forest Service (USFS). During the mid-1930s,
Robinson carried out an ambitious survey of condors in the National
Forests of southern California and assembled an impressive amount of
information on distribution, numbers, and biology of the species. The
importance of the Sespe and Sisquoc regions to condors was first given
general recognition in these studies, and Robinson, together with Robert
Easton, was instrumental in persuading the USFS to establish a formal
485 ha condor sanctuary in the Sisquoc area in 1937. Robinson's studies
were summarized in a number of internal USFS reports (Robinson,
1936a,b, 1939, 1940) and, when Koford began studies in 1939, he was
able to use this information to great advantage. Koford's debt to Robin-
son was a large one. For example, Koford's renowned estimate of 60
condors in the wild was preceded and may well have been influenced
by Robinson's estimate of 60 condors in the Los Padres National Forest
in 1934, a fact known to probably no more than a handful of people
alive today.
Another individual active at the same time, who was also of con-
siderable importance to the history of condor studies, was J. R. Pem-
berton, a Los Angeles geologist and wildlife photographer. Although
he never published more than brief notes on the species, Pemberton
eagerly pursued its habits, especially during the mid-late 1930s, and
recorded on motion picture film some remarkable scenes of nesting
behavior and mass feedings at carcasses. Pemberton's footage, together
with additional footage taken by Ed Harrison during the same period,
on file at the Western Foundation of Vertebrate Zoology (WFVZ), rep-
resents a classic documentation of the condors of that era. Pemberton
also served as a patron of Koford's early studies.
2.2. The Koford Era

The systematic studies begun by Carl Koford in 1939 led to many
important advances in knowledge of the range and general biological
characteristics of the condor. Koford was first a student of Joseph Grin-
nell and later of Alden Miller after Grinnell's death, and he absorbed
with dedication the field techniques of his mentors. Koford's field notes
are models of objectivity and meticulous detail, and he applied himself
with zeal to the task of gaining an understanding of a species that has

always been very difficult to study. Considering the logistic difficulties
he faced (he did not even have an automobile for the first year of study
and had to hike formidable distances repeatedly), the fact that he was
able to accomplish as much as he did was remarkable. Nevertheless,
many questions simply were beyond the capacities of a solitary worker
to resolve, especially with the tools then available for research.
Over his 4 years of intensive research (1939-1941, 1946), Koford
followed the reproductive biology of a number of condor pairs. The
most intensively studied pair was one of 1939 that he watched from a
distance on a regular basis through most of the incubation, nestling,
and postfledging periods. Other nests were studied primarily by peri-
odic visits to the nest caves themselves. By comparison with nesting
pairs that we studied intensively in recent years, the one pair Koford
studied intensively was atypical, with very frequent changeovers be-
tween adults at the nest and chronic hesitancy of adults in entering the
nest. To what extent this may have been due to the high levels of
disturbance that characterized this nesting effort is unknown, but the
nest was successful regardless.
Although Koford made no specific calculations of nesting success,
he assumed roughly 50% success in population projections, and ex-
amination of his monograph and field notes indicates that the nests he
found were indeed about 50% successful from the egg stage (see Snyder,
1983). Causes of nesting failure were for the most part uncertain. Eggs
broken by unknown agents were found in three, possibly four nests.
The chick in another nest suffered a broken wing, which later appar-
ently caused its death. This injury may have been a result of handling
during banding, judging from Koford's field notes. At another nest that
Koford entered on a near-daily basis for a period of several weeks prior
to hatching, the eggshell became punctured, and the chick did not make
it through the hatching process. Koford attributed this failure to the
activities of a nearby trail crew, although it could as well have resulted
from his frequent nest visits or may have been an entirely natural failure
due, for example, to ravens. At still another nest, studied by Telford
Work, Al Wool, and Harold Hill in 1945, the chick died of unknown
causes late in the nestling period. Koford (who never visited this nest
while it was active) later surmised that the nest might have been lost
at least in part because of human disturbance (the nest was visited a
great number of times), but actual evidence for this conclusion is ap-
parently nonexistent.
Koford obtained no information on what fraction of the adult pop-
ulation was attempting breeding. This is as important a question as

nesting success in understanding overall productivity, but in practical
terms it was one of the questions that was simply beyond reach at the
time.
In addition to nesting studies, Koford made trips throughout the
condor range, interviewing people familiar with the species and ob-
serving the birds feeding, roosting, and interacting with other scaven-
gers. This effort, building on earlier efforts of Robinson, led to the first
comprehensive picture of the condor's distribution and the first com-
prehensive identification of principal nesting areas, roosting areas, and
flyways.
His published conclusions as to the causes of overall decline (Ko-
ford, 1953) were less definitive than they are often portrayed. About
potential reproductive problems he said little, emphasizing only that
the intrinsic rate of increase was very low (he was unaware of replace-
ment clutching and doubted the existence of annual nesting). And even
though nesting success was reasonably good during his studies (despite
high levels of distrubance at several nests), he expended considerable
space discussing potential detrimental effects of human disturbance on
reproduction.
As to mortality factors, he provided mainly a list of known causes
of death, but aside from an emphasis on wanton shooting and past
museum collecting, he declined, quite properly, to identify which mor-
tality factors were most important and did not specifically address the
question of whether mortality factors were the main cause of decline
(he believed the population had been stable for about 30 years). His
remarks on the potential effects of 1080 poisoning were very circum-
spect, in contrast to the later emphasis given this toxicant by the McMillan
brothers. Koford stated quite clearly that although he had watched
condors feeding on 1080 poisoned ground squirrels (Citellus beecheyi),
there was no sign that they suffered any ill effects, although he did not
consider this conclusive evidence that they were unaffected. To this
day, there has not been a single well-documented case of a condor
adversely affected by 1080.
Otherwise, in his remarks on conservation, Koford cautioned against
further photography of the species and voiced his support for the es-
tablishment of sanctuaries to minimize disturbance to nests and roosts.
The Sespe Sanctuary, established in 1946 in the Los Padres National
Forest north of Fillmore, was a direct result of his studies. This mag-
nificent region of sandstone cliffs and canyons was Koford's principal
study area and encompassed many of the known condor nests.
Koford also warned against captive breeding, as he was extremely

doubtful that captive-reared condors could be successfully reestab-
lished in the wild. Similarly, he opposed artificial feeding programs,
which he believed would run risks of concentrating condors in areas
in which they could be wiped out by disasters and could cause birds
to lose the fear of man they needed for survival. Overall, Koford's
approach was one of recommending reductions of nearly all conceiv-
able threats to the species in the wild, coupled with an aversion to
anything hinting of direct human management.
Where he drifted into difficulty was in estimating numbers of con-
dors in the population (an essentially impossible task at the time, given
the sorts of data he had available). Possibly responding in part to Ro-
binson's earlier estimate of 60 individuals in the Los Padres National
Forest, Koford put forth his well-known figure of 60 condors, which
then became dogma for decades, despite the fact that the logical un-
derpinnings of this estimate were not presented in a full and compre-
hensive manner, as discussed in Snyder and Johnson (1985a,b), and
Johnson (1985).
Essentially all recent researchers tackling the condor numbers
question (e.g., Sibley, Wilbur, and ourselves) have come to the conclu-
sion that Koford's estimate was a gross underestimate of true numbers.
In fact, in order to arrive at his estimate, he had to reject one particular
single-day composite count by two members of the California Depart-
ment of Fish and Game in 1942 that totalled some 122 birds. This
rejection was a source of some early conflict between the California
Department of Fish and Game and Koford's followers (we will return
to this issue in more detail in the section on establishment of the Sespe
Sanctuary). In our judgement, Koford very likely had been dealing with
a population somewhere in the vicinity of 120 to 180 individuals (see
Snyder and Johnson, 1985a,b; Johnson, 1985), an estimate that matches
closely an unofficial 150 + bird estimate offered by the California De-
partment of Fish and Game during the early 1950s (McMillan, 1953).
Koford's own recognition of the possibility that there might be more
than 60 condors in the population was clear from statements in his
doctoral dissertation (Koford, 1950): "If my estimate of 60 condors is
in error it is too conservative. If there are 100 condors, so much the
better for the survival of the species." For unknown reasons, these
qualifying remarks to his population estimate did not appear in his
published monograph, leading followers to attach a significance to the
60-bird figure that simply was not warranted. The many and varied
political repercussions of this population estimate are considered later
(Section 3.1).
2.3. The McMillan Years

Following Koford's study and the establishment of the Sespe Sanc-
tuary, there was considerable hope that the decline of the species might
be arrested. The USFS and NAS sponsored a succession of patrolmen
for the sanctuary who made efforts to monitor condor numbers and
nesting, but the data collected were of very uneven quality. By the late
1950s and early 1960s, concerns were being raised that condor numbers
were still declining, and in 1963 and 1964 the NAS, together with the
National Geographic Society, sponsored a follow-up study to Koford's
efforts. Performing the field work were two rancher friends of Carl
Koford, Ian and Eben McMillan, while Alden Miller at Berkeley pro-
vided academic input to the enterprise by supervising the planning,
data analysis, and writeup of results.
This study was run very differently from Koford's in a number of
respects. First, no effort was made to find and study nests, a response
in part to Koford's admonitions regarding the dangers of human dis-
turbance at nests. Thus, there was no direct evaluation of reproductive
health of the population. In addition, the fieldwork pursued was largely
limited to an effort to evaluate the gross availability of food, to collect
data on condor numbers and distribution, and to accumulate infor-
mation on mortality threats to the species. In this effort, Miller et a1.
relied heavily on interviews of other ranchers, USFS employees, and
other individuals.
In their summary report, Miller et a1. (1965) concluded that whereas
there had been 60 condors in Koford's day, there were now only about
40 birds and that this decline was not attributable to reproductive prob-
lems but to excessive mortality from shooting and poisoning. They were
confident that food was no problem.
The population estimate of 40 individuals was based largely on
comparisons of sizes of the largest flocks these researchers could doc-
ument with the largest flocks documented by Koford; thus, the accuracy
of their estimate depended crucially on the accuracy of Koford's esti-
mate. Unfortunately, like Koford, they encountered one sighting made
by someone with good credentials that appeared to be larger than their
total population estimate. How they handled this sighting is worth
considering in some detail, as it has been a source of strained relations
between the individuals involved for more than two decades.
The sighting in question was made by Bert Snedden, a rancher in
the southern San Joaquin Valley foothills, who has known condors all
his life (some of his early sightings were recorded by C. S. Robinson).
Snedden reported to the McMillans that in the fall of 1961 he and his
sons observed a total of 63 condors, in two groups, circling over his

ranch at one time. When this sighting appeared in Miller et 01 (1965),
however, the total given was only 33 birds, with no discussion of the
discrepancy between what Snedden had told them and what they re-
ported.
In treating interview data, one normally chooses between accepting
or rejecting a record, depending on how one evaluates the reliability
of an observer. Crediting one part of Snedden's sighting but not the
other part is an approach we find difficult to understand. For if one
believes he was competent to identify 33 condors, why not the other
30? Conversely, if one believes he misidentified 30 birds, why would
one have any confidence in the other 33? Snedden to this day (personal
communication) vigorously asserts that he counted 63 birds four times
as they circled overhead and that they were all condors. We know of
no reason to reduce or reject his count. The McMillan brothers (personal
communication) have declined to comment on their treatment of this
sighting.
Our own evaluation of the population estimate of Miller et 01., as
presented in Snyder and Johnson (1985a,b) and Johnson (1985), is that
since it was based primarily on comparisons of flock sizes between
their study and Koford's study, it probably was subject to about the
same error factor as Koford's estimate, a factor of about two to three.
Thus we would estimate that the actual condor population during the
Miller et al. study was somewhere between 80 and 120 condors.
Although Miller et 01. spent a considerable portion of their paper
assembling anecdotal and direct evidence of shooting threats to the
condor, perhaps the most interesting aspect of their study was their
discussion of possible causes of death of three condors recovered in
three different areas near Granite Station of Tulare County during the
early 1960s. No broken bones were found in any of these birds, nor
were there other signs that they had been shot. But in one case, when
the head of the dead bird was placed in a dermestid colony for cleanup,
it promptly exterminated the colony, a fact strongly suggesting to Miller
et al. that poisoning was the cause of the condor's death. This condor
had hung in a barn for several years before Miller et a1. obtained it, so
it was quite dried out, although there was still some meat in the skull.
However, unknown to Miller et aI., but later determined by Ben Easley
(F. Sibley, personal communication), the condor carcass had been de-
liberately sprayed with DDT as it hung in the barn to keep down the
flies. This provides an alternative explanation for the death of the der-
mestids.
CONDOR BIOLOCY AND CONSERVATION 187
The other two condors picked up dead or dying near Granite Station
were also potential cases of poisoning, but no definitive residues of
poison were ever found in any of the birds. The McMillans nevertheless
strongly suspected 1080 involvement in these deaths mainly because
the birds were found in areas of 1080 squirrel poisoning, and to this
day they have campaigned against this chemical as a threat to condors.
It is quite possible, however, that if these condors were poisoned, which
does not seem unlikely, the poison involved may well have been some-
thing other than 1080. Lead poisoning was neither looked for nor ruled
out for these cases and, as we now know from evidence of the 1980s,
this has been a very important source of mortality that has almost
certainly been killing condors for centuries. The symptoms seen in one
of the three birds prior to death-emaciation and lack of coordination-
are typical of lead poisoning. Another possibility was strychnine poi-
soning, though strychnine is usually fast-acting enough that poisoned
animals do not get far from the scene of poisoning, and these condors
were not found next to poisoned carcasses.
Although we agree with the Miller et al. assessment that the major
cause of decline for the condor has been mortality factors, the way in
which they reached this conclusion is not convincing in the light of
current knowledge. By analysis of sightings in the field, they concluded
that there were a minimum of 10 different immature condors in the
wild during their study, and since their total population estimate was
40 birds, they concluded that about 25% of the population was made
up of immatures, to them a healthy fraction that indicated the species
was not having reproductive problems. Therefore, the problems had to
be ones of mortality. However, if (as we believe) the total condor pop-
ulation during the Miller et a1. study was actually 80-120 birds, these
researchers were actually accounting for a minimum of only about 10%
of the population as immatures, which is hardly conclusive evidence
of reproductive health of the population. Nevertheless, there could well
have been more than 10 immatures alive in the population at the time.
The methods of observation used by Miller et a1. were much too crude
to rule this out; in fact, the ratios of immatures to adults they saw in
some flocks suggest that this could have been true. Thus, it is very
possible, although undemonstrated, that condors were reproducing nor-
mally at the time.
In summary, neither Miller et a1. nor Koford had obtained the sort
of data necessary to establish conclusively whether the decline of the
condor was being caused primarily by reproductive problems or mor-
tality problems, or a combination of the two. Although many bits and
pieces of information had been collected on factors stressing the species

in various ways, there was as yet no true understanding of what the
major forces were that were driving the decline.
2.4. The Sibley Years

During the mid-1960s, the integrity of the Sespe Condor Sanctuary
was threatened by proposed dams along Sespe Creek above Fillmore.
The USFWS responded by sending Fred Sibley to California to evaluate
potential impacts of the proposed dams on condors. As one of the first
field biologists of the newly created Endangered Wildlife Research Pro-
gram, Sibley's approach to the dam issue was to launch a massive effort
to locate active and inactive condor nest sites, both in the path of the
proposed project and elsewhere, to characterize the features, especially
various human disturbance factors, that might define whether sites were
usable by condors. In this effort, Sibley located a large number of condor
nests. Most were old inactive sites that he found by following up on
old accounts of egg collectors and by systematic rope work on cliffs.
Each site found was carefully measured, mapped and evaluated by a
diverse set of criteria. Collaborating on a part-time basis in this and
other condor research projects were John Borneman and Dean Carrier.
Borneman had been appointed condor warden for the NAS in 1965,
following recommendations of Miller et a1. that such a position be
established. Carrier was the first USFS condor biologist and began stud-
ies in 1968.
The result of the nest-investigation efforts was a thorough report
on predicted impacts of the proposed Sespe dams on condor repro-
duction (Sibley, 1969). Sibley found no active condor nests within
specified distances of various disturbance factors, such as paved roads.
Whether this was a result of elimination of condors nesting too close
to disturbance, a result of responses of the birds to disturbance, or only
a chance effect was unclear, but this was in a sense immaterial, as the
prudent response was to create safety zones around active and recently
active sites. As the proposed dams and associated developments fell
within critical distances of a number of active and recently active con-
dor nests, Sibley'S report predicted significant impacts of the project.
But even before Sibley'S report was published, the Sespe dams project
was shelved because local residents failed to approve a bond issue
necessary for the project to proceed.
Sibley was also a central figure during the early years of the annual
October Survey, a giant simultaneous count of condors from strategic
lookouts throughout the known range. The survey was initiated in 1965
CONDOR BIOLOGY ANIl CONSERVATION 189
by Bob Mallette of the California Department of Fish and Game (CDFG)

and by John Borneman of NAS (Mallette and Borneman, 1966); it con-
tinued each year through 1981, with the exception of 1979. Although
procedures were originally designed to yield a minimum estimate of
population size on a standardized basis, counts turned out to be quite
variable from one year to the next, presumably because of weather
influences, changes in foraging patterns of birds, changes in numbers
of observers and lookouts, and other factors. There were also some
difficulties in determining whether birds seen at one lookout might be
the same as ones seen at another lookout at a different time, and hard
decisions had to be made in coming up with total numbers of birds
seen.
Nevertheless, despite some uncertainties to the counts, they did
serve to give some idea of minimum size and overall trends of the
population. During the late 1960s, counts generally exceeded 50 in-
dividuals, though they had dropped to less than 20 individuals by the
early 1980s. Mainly on the basis of the survey, Sibley believed that the
wild population consisted of about 60 individuals during the late 1960s.
This estimate was identical to Koford's estimate for the 1940s but,
although this suggested population stability to some observers, it was
obvious that many fewer birds were then being seen in all parts of the
range than what Koford had observed, and Sibley (personal commu-
nication) believed that Koford may have actually had as many as 200
condors alive in the wild during his study.
The McMillans consistently challenged the results of the October
Survey and Sibley's conclusions and continued to maintain that their
estimate of 40 birds for the early 1960s was valid. Our own judgment
is that Sibley's population estimate was a good one, as one can arrive
at roughly the same estimate by comparing flock sizes seen during his
studies with flock sizes seen in more recent years (when population
size was finally known accurately). The October Survey was abandoned
in 1982, when a comprehensive method of censusing condors through
systematic photography of flying birds and identification of individuals
was developed (Snyder and Johnson, 1985a,b).
Condor nesting success continued to run close to 50°;', through the
Sibley years, although egg breakage was frequent and shells collected
by Sibley averaged very thin (Kiff et a1., 1979; Snyder, 1983; Snyder et
a1., unpublished data). However, the extent to which breakage was
caused by shell thinning or by other factors was not determined, and
the rate of breakage did not differ significantly from the rate of breakage
during the pre-DDT (Koford) years.
It was not yet possible to estimate what fraction of the adult pop-
ulation was attempting to breed. Despite Sibley's great success in lo-

cating nests, it is quite clear from more recent information that he did
not find all active pairs (this was much too large a task for the limited
manpower available in those days). However, Sibley's efforts were suf-
ficient to establish that use of the Sespe Sanctuary by breeding pairs
continued to be reasonably strong and that a considerable number of
pairs were nesting outside the Sanctuary as well.
Only one dead condor was found during the Sibley years (a chick
that fell from its nest cave), while population counts and determinations
of productivity were still too crude to permit calculations of overall
mortality rates. However, one starving fledgling was recovered in Feb-
ruary 1967 when it wandered into a summer homes area in Matilija
Canyon (it may have been starving because of reluctance of the adults
to enter the developed area). Sibley and Borneman attempted to release
the bird again to the wild after feeding it back to a vigorous condition,
but they were unsuccessful, and the bird was ultimately made a per-
manent captive at the Los Angeles Zoo. For the next 15 years this bird,
"Topatopa," was the only California Condor in captivity. Overall, Sib-
ley did not hold strong views about the causes of the decline, although
he was concerned over the possibility of food shortages limiting repro-
ductive effort, a concern that was tested on a large scale by his successor
in the Endangered Wildlife Research Program of the USFWS, Sanford
Wilbur.
2.5. The Wilbur Era

A primary focus of Sanford Wilbur's research was an experimental
attempt to increase condor reproduction in the Sespe Sanctuary by
providing a good food supply nearby (Wilbur et. 01., 1974; Wilbur,
1977). The feeding effort was started in 1971 and continued right into
the 1980s, as pursued by Mike Silbernagle of the Hopper Mountain
National Wildlife Refuge in recent years. Carcasses of large vertebrates,
primarily deer and goats, were provided throughout the year on a once-
weekly basis from 1971 to 1973 and on a twice-weekly basis from 1974
to 1977; indeed, these carcasses received considerable, if irregular, con-
dor use over the years. Nevertheless, although use was heavy at times,
it was never sustained for long and, in overview, the program never
resulted in the condor population becoming dependent on the food
provided. Nor did it produce any clear evidence for increased repro-
duction in the Sespe Sanctuary. Quite clearly, the condors had many
other sources of food available to them and continued to forage mainly
in other areas, evidently receiving regular reinforcement to do so by
CONDOR BIOLOGY AND CONSERV AnON 191
presence of food in these other areas. Thus, the feeding program gave
no good evidence for food limitations in the species.
Perhaps the most unfortunate aspect of these experimental results
was not so much that the feeding program was unsuccessful in achiev-
ing its stated goal, but that the results were later disregarded as the
whole issue of feeding condors arose again in the crisis period of 1985,
a topic we consider in detail in Sections 3.4.1 and 3.4.2.
Wilbur also made a strong effort to arrive at good estimates of the
condor population size, and indeed we believe his estimates of 50-60
birds in 1968 and 25-35 birds in 1978 (Wilbur, 1980) were excellent,
although recent evidence shows that some of his assumptions were not
entirely justified. By a close examination of records of condor sightings,
Wilbur came to the conclusion that there were actually two populations
of condors in existence, a Sespe-Sierra population and a Coast Range
population, with the boundary between the two running roughly along
the Ventura County-Santa Barbara County line. It was his assessment
that these populations did not normally mix and thus could be con-
sidered separate entities in combining counts to arrive at total popu-
lation estimates.
With the benefit of post-1981 abilities to identify individuals through
photography, and later telementry, we can now say that Wilbur was
only partly right. While adult condors nesting in the Sespe region es-
sentially never crossed the county line to appear in nesting areas in
Santa Barbara County, and vice versa, these same birds did mix freely
on the foraging grounds in the San Joaquin Valley foothills, and indeed
every bird in the population, whether from the Sespe-Sierra region or
the Coast Range (Santa Barbara) region, was documented using virtually
the entire foraging range-a giant J-shaped region bordering the south-
ern San Joaquin Valley (see Snyder and Johnson, 1985a,b).
Nevertheless, Wilbur was quite justified in considering birds counted
in the Sespe Sanctuary as being different from birds counted in the
nesting areas in Santa Barbara County (at least adults). Although there
was only one condor population, adult movements from all nesting
areas were normally confined to direct commutes to the nearest portion
of the foraging range in the San Joaquin Valley foothills, and thence
up and down the foraging grounds, and finally back to the same specific
nesting areas in the mountains from which they originated (Fig. 1).
Thus, adults, unless they were unpaired individuals looking for mates,
did not normally move along the mountain ranges from one nesting
area to another parallel to the foraging range. By contrast, immatures
wandered much more unpredictably throughout the range of the spe-
cies, including all the nesting areas. The mix of birds of all ages on the
I---~
\ \
\ -,
50 K 110m.!.,. I
FIGURE 1. Approximate limits of the California Condor range during the modern pro-
gram, illustrating known nest sites (solid dots), principal foraging grounds (bounded by
the dotted line), principal sanctuaries, and usual routes of travel of two recent pairs from
their nesting areas to the foraging grounds.
foraging grounds was quite thorough, though there was a tendency for
adult birds to be found in parts of the foraging range closest to their
nesting areas.
The important point to emphasize is that whereas Koford (1953)
assumed that any bird seen in the Sespe Sanctuary in Ventura County
could be the same as any bird seen in the Sisquoc Sanctuary in Santa
Barbara County the next day, we now know this to have been highly
unlikely (and limited mainly to immatures); this explains, at least in
part, why Koford's population estimate was so low.
Overall, Wilbur (1978) concluded that the main cause of the recent
decline in the population was a breakdown in reproduction, not in
nesting success but in a failure of many pairs to attempt breeding.
However, an overall failure of pairs to attempt breeding is difficult to
prove unless one is carefully monitoring.all nesting areas in the early
breeding season, an enormous task. Wilbur did not actually document
any nonbreeding pairs, and in examining his field records we believe
that his conclusion was primarily a consequence of the fact that his
research efforts were concentrated so heavily in the Sespe Sanctuary
region, while he gave low priority to comprehensive checking of known
and potential nesting areas elsewhere. Condor reproduction in recent
years has been taking place primarily in other regions and, as discussed
by Snyder (1983) and as has been confirmed in great detail in subse-
quent years, the remnant population, at least since the late 1970s, has
not been suffering from an appreciable shortage of breeding effort. We
know of no reasons to believe that the situation might have been dif-
ferent in the early 1970s. In fact, there is strong evidence that at least
four of the nesting territories we found active during the 1980s in
regions outside the sanctuary were also active and producing young
during Wilbur's study, yet were not reported in his nesting summaries.
One of Wilbur's contributions was the assembly of all known rec-
ords of mortality in the wild population (Appendix II of his 1978 mono-
graph). Causes of death were unknown in a considerable fraction of the
records, but of the accurately dated records in which a cause had been
identified (rightly or wrongly), shooting looms as the most important
cause, accounting for 38 cases overall and 44% of the total records
(excluding museum collecting and other purposeful collecting). This
finding gives apparent support to the emphasis given shooting by Ko-
ford (1953) and Miller et a1. (1965).
Nevertheless, it is important to recognize that Wilbur's list may
suffer from strong biases, especially those influencing whether or not
a dead bird is likely to be recovered. In the case of the condor, shooting
may be a source of mortality that is likely to be detected for several
reasons: (1) at least historically, shot birds have often been kept and
displayed (e.g., as taxidermy mounts, on sides of barns, on fences); (2)
birds that are abandoned by shooters are relatively likely to be found
by others, as most shooting takes place close to roads, trails, and so
forth; and (3) shooting is a cause of death that is relatively likely to be
diagnosed because of such factors as obvious wounds and broken bones.
By contrast, birds dying from certain kinds of poisoning, especially
slow-acting poisons such as lead, are extremely unlikely to be re-
covered, as they may die anywhere in the range, with no particular
reason for them to expire in areas in which they are likely to be found.
Furthermore, until very recently, very few condor carcasses had been
chemically analyzed for residues of poisons. Thus, even though a large
fraction of mortality of the species might conceivably be caused by lead
poisoning, one would not expect this to be visible in a listing such as
Wilbur's, and it isn't. Clearly, one cannot conclude very much about
which mortality factors are truly important for the species from dead
condors found by chance and subjected to nonstandardized postmortem
examinations. While we do not wish to minimize the probable impor-
tance of shooting, one cannot even legitimately conclude from Wilbur's
list that shooting has been a major source of mortality, let alone the
major cause. It is important to emphasize that the records listed by
Wilbur represent only a very tiny fraction of the condors presumably
dying during the period considered, and very likely a highly biased
fraction.
In summary, despite the many years of very important and admi-
rable research by Wilbur, Sibley, Miller et al., and Koford, the causes
of decline of the species were still not well understood by 1980, not
even to the extent that one could be confident that the major factors
were indeed mortality factors rather than reproductive factors. In large
measure, this unfortunate situation was not the fault of the researchers,
but of the difficulties in resolving these questions because of (1) the
extremely wide-ranging habits of the species and great practical diffi-
culties in finding nests by conventional methods, (2) great practical
difficulties in obtaining an accurate census of the population, (3) in-
sufficient manpower and resources available to even attempt resolution
of some research questions, and (4) political restraints that placed cer-
tain powerful research methods "off limits" (especially radiotelemetry
and visual marking of birds for individual identification), primarily
because of fears that the methods would in themselves endanger the
species. These fears even led at times to the extreme point of view that
passive observations of nests from considerable distances were unac-
ceptably risky.
Yet, without good answers to the question of what was causing the
decline, there could be little hope of reversing the decline. The con-
servation measures tried since the 1930s had clearly been ineffective
in arresting the approaching extinction of the species.
2.6. The Modern Research Program

In early 1980, an expanded intensive condor research program was
initiated by biologists of the newly formed Condor Research Center
(CRC) in Ventura. This was primarily a joint effort of the USFWS and
the NAS, led by NFRS of the USFWS and John Ogden of NAS, but it
received support as well from the USFS, the CDFG, and the Bureau of
Land Management (BLM). Many other organizations and individuals
came to play important roles in the program in subsequent years. The
impetus for this program was a widespread recognition that the condor
was rapidly being lost and that much more intensive research methods
were needed to elucidate the problems causing the decline and to devise
effective conservation strategies. It was also finally recognized that there
was an urgent need to establish a viable captive population, in the
event that efforts to save the wild population might fail. Although the
birth and many lives of the modern program are a complicated tale of
the interaction between biology and politics, we focus in this section
only on biological questions.
As originally planned, the new program would proceed on a broad
front, including both traditional and new intensive approaches. Five
principal thrusts were envisioned: (1) efforts to improve censusing of
the wild population, primarily through radiotelemetry; (2) intensive
studies of reproduction, primarily through systematic efforts to locate
and study active nests using expanded traditional methods aided by
radiotelemetry; (3) efforts to study mortality, primarily through radi-
otelemetry; (4) efforts to study habitat requirements, primarily through
radiotelemetry; and (5) efforts to form a captive population, primarily
by trapping nonbreeding adults (if they could be identified as such)
and immatures. As it turned out, several of the main goals were achieved
by methods other than those originally envisioned, in part because of
delays in initiation of radiotelemetry and in part because of develop-
ment of superior alternative methods as the program evolved.
2.6.1. Censusing
Until late 1981, condor censusing efforts were limited to the annual
October Survey, but whereas a minimum of 19 birds were documented
on the survey in 1980, only 11 (possibly 12) turned up on the 1981

count, and this latter count was known from other information to be a
gross underestimate of the total population. It was clear that the survey
was continuing to be an inconsistent method for counting condors.
However, in the summer of 1981 a much better method had its
beginnings in a project of Eric Johnson and his students at California
Polytechnic State University, San Luis Obispo. These observers had
located what proved to be an excellent condor observation point along
a road overlooking part of the foraging range in the southern San Joaquin
Valley foothills. From here, they were able to make daily observations
of condor behavior patterns (Johnson et 01., 1983); in addition, they
attemped to keep records of the flight-feather molt patterns of each bird
seen. It soon became apparent from differences in molt patterns that
these observers were not just looking at the same individual condors
day after day, but at a great variety of different individuals. In fact, over
a period of several weeks, it appeared that they might be observing a
large majority of the birds left in the wild. However, it was also apparent
that there were difficulties in visual recordings of molt patterns. It was
often hard to see all features accurately in the time a bird was in view,
and there were occasional problems with confusion between left wings
and right wings in the recording process.
In the fall of 1981, we began a collaborative effort with Johnson
and others to study flight-feather patterns of individual condors pho-
tographically. This proved a much more satisfactory way to record data.
From early 1982 on, field workers in the program routinely carried
cameras with powerful telephoto lenses to photograph condors in flight
whenever there was an opportunity to do so anywhere in the range of
the species. We were also fortunate to receive many photographs con-
tributed by individuals outside the program. This effort led not only
to a rigorous method for censusing the remnant population, but gave
as well a wealth of detailed information on movements of birds, their
molt patterns, and their timing of disapperance (Snyder and Johnson,
1985a,b; Johnson, 1985; Snyder et 01., 1987).
So whereas we had originally anticipated that accurate censusing
might only be possible with extensive radiotelemetry or other marking
of birds, this did not prove to be the case. In fact, intensive photographic
efforts also yielded important information on other research topics for
which we had expected radiotelemetry to be essential, especially de-
terminations of home ranges and mortality rates.
Minimum summer condor counts derived from photocensusing for
1982 and the three following years were 21, 19, 15, and 9 individuals,
respectively. Although we originally estimated that we might have missed
CONDOR BIOLOC;Y AN)) CONSERVATION 197
as many as three individuals on each count, we now suspect that we

were much more accurate than this and may have documented the
population size exactly during these years. No previously unknown
birds ever turned up after 1983.
2.6.2. Reproductive Studies

A large-scale effort to check all recently active condor nesting areas
and other potential nesting areas was begun in 1980. This effort soon
yielded two active pairs that had not been studied earlier; in succeeding
years, several more previously unknown active pairs were located. With
few exceptions, these newly documented pairs were apparently not
really new pairs but pairs that just had not been recognized earlier. All
the newly found pairs were located in regions outside of the Sespe
Sanctuary, except for a pair formed in 1986, which included the female
from Wilbur's Sespe Sanctuary pair. Her previous mate had died over
the winter of 1984-1985.
From 1982 onward, intensive studies of nesting pairs in conjunc-
tion with intensive photographic efforts permitted a near-complete de-
termination of the reproductive status of all individuals in the popu-
lation (Table I). Not all pairs documented in this period were egg-laying
pairs; in fact, two pairs studied in 1981-1983 demonstrated an inability
to perform successful copulations, although they investigated nest sites
and went through other reproductive behavior patterns in an apparently
normal fashion. We suspected that these pairs might in fact be homo-
sexual pairs because the identity of individuals on top in copulations
was not consistent and because both members of both pairs gave court-
ship displays. Unfortunately, both pairs lost members before a program
to trap, sex, and radio tag wild birds was finally underway, so conclu-
sive evidence of sex is lacking for two of these birds. The surviving
member of each pair was later determined to be a male.
The data in Table I, when considered in conjunction with extrap-
olations presented in Snyder (1983), do not suggest any significant
difficulties with reproductive effort, at least back to the late 1970s. Most
adults were paired and attempted breeding through this period. Massive
mortality greatly disrupted the makeup of pairs over the winter of
1984-1985, so the relatively low percentage of birds paired and breed-
ing in 1985 and 1986 was not surprising. By 1986, there was only one
female left in the wild.
Calculations of nesting success for years covered by the modern
program are complicated by extensive manipulation of nests after 1982.
In the following analysis, we have included only (1) nesting efforts
TABLE I
Early Breeding Season Makeup of the Wild Condor Population
Bird classification 1982 1983" 1984 1985 b 1986
Total individuals 23 19 15 10 5
Breeding pairs 4 4 5 2" 1
Nonbreeding pairs
(homosexual males?) 2d 1 0 0 0
Unknown status pairs 1e 1f 0 0 0
Unpaired male adults 0 0 2 2 3
Unpaired female adults 1 1 1 2 0
Unsexed, unpaired adults 2 1 0 0 0
Immatures 6 5 2 2 0
Percentage adults paired 82 86 77 50 40

Percentage adults in
breeding pairs 47-59 57-71 77 50 40
"From 1983 onward, all eggs and nestlings were removed for the captive breeding program.
bMortality of five adults over the winter of 1984-1985 disrupted four breeding pairs.
'The male of a new pair was lost early in the breeding season. Although no egg was laid, the pair
was ranked as a breeding pair because it was known to be heterosexual and copulations were
proficient.
dOne member of one pair (unknown sex) was lost in the breeding season.
'Only one member of the pair was photographed and sexed (female); her mate apparently was lost
during the breeding season, and their nesting area was never located.
{Observed as a pair but their nest was not located in 1983 and it was not clear that they nested (new
pair). The same pair in 1984 laid a fertile egg.
observed at the egg stage that were allowed to proceed at least to the
late nestling stage or to failure, and (2) nesting efforts observed at the
egg stage, which we planned to leave unmanipulated through to fledg-
ing but from which we removed eggs to captivity as the obvious threats
to success in the wild would almost certainly have caused failure of
the nests. These latter nests are ranked as failures, although surviving
young were produced in captivity in all cases. Since known natural
failures have been very rare past the mid-nestling stage (Snyder, 1983),
we have also included as successes three nests from which we took
nestlings into captivity and one nest from which we lost a chick in a
handling accident in 1980. However, we have ranked as uncertain in
outcome a nest from which we took a nestling into captivity in 1982,
because disappearance of an adult of the pair (the bird later returned)
and low feeding rates were the reasons for capturing the chick. The
foregoing decisions have been made in an effort to come as close as
possible to an unbiased estimate of natural nesting success of egg-laying
pairs.
The data so treated yield either seven or eight nests successful out
CONDOR BIOLOGY AND CONSERV A nON 199
of 17 between 1980 and 1985, or 41 to 47% nest success, a value very

similar to the historical rate (Snyder, 1983) and to that of other cathartid
and Old World vultures (Jackson, 1983; Mundy, 1982). Thus, there were
no clear indications from either reproductive effort or reproductive
success that the remnant population was having significant difficulties
in breeding.
Unquestionably, the most significant finding resulting from inten-
sive nest observations was the fact that California Condors will rou-
tinely lay replacements for eggs lost early during the breeding season.
This capacity was first observed conclusively in 1982 following a case
of natural egg loss, and it was ultimately demonstrated in four of the
five pairs from which eggs were taken to establish a captive flock (Sny-
der and Hamber, 1985). In fact, three different pairs demonstrated an
ability to lay not only two, but three, eggs in a single breeding season.
The normal recycling time was about 1 month after egg loss and, in all
cases we observed, replacements were laid in different nest sites from
the ones in which previous eggs had been laid. The only known ex-
ception to the rule of pairs switching sites to lay replacements was a
nest of 1939, in which Koford found a remarkably young nestling late
in the year. Unknown to Koford, M. C. Badger had collected an egg
from the same site early in the same year, a fact that surfaced only in
1977, when Badger's egg collection came to the WFVZ (Harrison and
Kiff, 1980). Although it cannot be proved that the same pair of condors
laid both of the 1939 eggs, this seems likely.
In addition to replacement clutching, two cases were documented
of condor pairs breeding in successive years with concurrent survival
of fledglings, Le., annual nesting. In both cases, however, fledging of
chicks was early in the first year and egg laying came late in the second
year, so it does not appear likely that true annual nesting may commonly
occur in strings of more than 2 years (Snyder and Hamber, 1985).
Taken together, the capacities for replacement-clutching and an-
nual nesting mean that total productivity of the population will be
underestimated if calculations assume only one nesting attempt per
pair per year if the attempts are unsuccessful, or one attempt per pair
every 2 years if the attempts prove successful. Just how much of an
actual increase in productivity over these assumptions occurs under
natural conditions is not determinable from existing data and depends
critically on how often failures occur early enough in the breeding
season to allow replacement attempts. If one were to assume that (1)
perhaps one half the nesting failures occur early enough to allow repeat
attempts, (2) annual nesting can only occur in years following suc-
cessful fledging of chicks from early eggs, and (3) nesting Sllccess in
individual attempts is 50% regardless of timing in the breeding season,

one can calculate that overall productivity of the population would be
equivalent to that of a population in which pairs always nest annually,
never lay replacements, and enjoy a nesting success of approximately
50%. Thus, the capacities for replacement clutching and annual nesting
may enhance the overall productivity of the population quite signifi-
cantly.
Nevertheless, we emphasize that we have seen abnormalities in
the reproductive characteristics of most recent pairs, which suggest that
all has not been completely well with reproduction in recent years.
Aside from the two pairs mentioned above with inabilities to copulate
successfully, one pair studied intensively from 1980 through 1984 had
chronic difficulties in coordinating nest exchanges between adults. After
egg laying, the female was rarely allowed access to her egg without
conflict with her mate, who appeared to want to conduct all incubation
himself and repeatedly drove her aggressively from the nest site. In two
nesting attempts the conflicts led ultimately to egg loss. While the
causes of this problem were unknown, it is important to note that
similar behavior has been seen on several occasions in captive pairs of
Andean Condors (Vultur gryphus) (M. Wallace, W. Toone, J. Carpenter,
personal communication).
Another recent pair of California Condors consistently laid abnor-
mally small eggs-smaller than ever recorded before for wild condors.
These eggs were also consistently thin-shelled (25-30% thinner than
the historical mean). Nevertheless, with the exception of one very thin-
shelled egg of 1986, the eggs of this female hatched well and produced
apparently normal chicks. Examination of all condor eggs for a rela-
tionship between egg weight and eggshell thickness has revealed a
strong positive correlation, and it is not clear that the eggs being laid
by this female were abnormally thin for their size (Snyder et al., un-
published data). Thus despite their thin shells, these eggs may have
been normal in resistance to damage, and there is no strong evidence
that these eggs were a cause of lowered fitness, though small eggs are
not equivalent to large eggs in a variety of characteristics affecting
fitness in many species (see Mead et al., 1987, and references cited
therein). All other pairs under study laid eggs close to normal in size
and eggshell thickness, so it does not appear that recent eggs in general
have been suffering from the DDE syndrome, although eggshells col-
lected during the 1960s were consistently thin, and one extremely thin-
shelled crushed egg of the above female in 1986 (44% thinner than the
historical mean) had high levels of DDE (see Snyder, 1986).
Still another recent pair produced abnormal offspring. Their fledg-
ling of 1981, now a captive, gapes chronically after mild exercise, a

trait not seen in other condors. Another of their chicks did not make
it through the hatching process successfully in 1984. This bird had only
half a skull and malformed limbs.
Finally, another recent pair exhibited recurrent problems with egg
hatchability, losing eggs at hatching in the wild in 1981 and in captivity
in 1984. Furthermore, a captive-hatched young from this pair in 1983
was very difficult to keep alive during the first few days, and one of
their eggs in 1985 suffered early embryonic death. Causes of lack of
vigor and poor survival of eggs and hatchlings of this pair are unknown.
Although the causes of the abnormalities of the above pairs are
uncertain, the fact that nearly every pair studied closely in recent years
has had reproductive abnormalities is noteworthy. We know of only
one closely studied egg-laying pair during this period that was free of
obvious difficulties, and one cannot help but wonder whether the lim-
ited gene pool of the remnant population may have been involved in
some or all of the problems. While many of the problems discussed
above did not cause nesting failure, and thus do not show up in re-
productive success statistics, such problems as these, depending on
how they progress in the captive flock, could prove to be a significant
hurdle for long-term survival of the species.
Aside from the intrinsic problems considered above, there have
been other causes for nesting failure. The principal natural enemy faced
by nesting condors in recent years has been the Common Raven (Corvus
corax). During 1982, we observed a raven destroying the egg at one site,
and in 1983 we obtained strong circumstantial evidence (condor egg-
shell in a nearby raven nest) that a second condor nest was similarly
preyed upon. In addition, we have observed numerous unsuccessful
attempts of ravens to steal eggs from virtually all recent condor pairs.
It seems very possible that ravens have been the principal cause of the
high rate of egg breakage seen through all eras (see Snyder, 1983). We
even found condor eggshell in an ancient raven nest adjacent to a condor
nest that experienced egg breakage during Koford's study (Snyder et
aI., 1986). Although they are highly aggressive toward ravens near their
nests, condors are relatively vulnerable to raven predation on their eggs
because of frequent lapses in nest attendance during nest exchanges
and because of their frequent use of shallow nest caves in which they
have been conspicuous to ravens.
Two other natural enemies have posed apparent threats to condor
nests-Golden Eagles (Aquila chrysaetos) and black bears (Ursus amer-
icanus). Although no successful cases of predation by these species
have been documented, several attempts have been witnessed, and the
highly aggressive responses of the adult condors to these predators

provide strong evidence of the severity of the threats posed. Other
nesting failures have been traceable primarily to structural defects in
nest sites, such as sloped floors or entrances that predisposed eggs and
nestlings to fall from the caves to destruction below (Snyder et 01.,
1986).
2.6.3. Mortality Studies

The data on causes of mortality up to 1980 were likely very highly
biased and could, if accepted at face value, lead to the wrong emphasis
in conservation efforts (see Section 2.5). We recognized early that rel-
atively unbiased information on dead and dying condors was a critical
need, and that radiotelemetry offered the only known practical way to
gain such information. In addition, we anticipated that intensive ra-
diotelemetry would be the route by which good data on overall mor-
tality rates would be achieved. As it turned out, the evaluation of overall
mortality rates came mainly through photocensusing efforts, and ra-
diotelemetry efforts came too late to offer more than highly suggestive,
although nonetheless crucially important, insights into major causes of
mortality.
Overall mortality rates, as calculated accurately from the photo-
census information, were exceedingly high. If we take March to March
as the annual period for calculation of mortality losses, 4 of 23 birds
(17.4%) were lost between 1982 and 1983; 4 of 19 birds (21.1%) were
lost between 1983 and 1984, 6 of 15 (40%) were lost or found dying
between 1984 and 1985; and 1 of 6 (16.7%) was lost between 1985 and
1986. For the 1982-1983 calculations, we have discounted one bird
taken into captivity in early December 1982. Likewise, for the 1985-1986
calculations, we have discounted three birds trapped into captivity in
the summer of 1985. Almost all mortality has occurred in the period
from late fall to early spring (Table II), so birds not passing through
this period should not be included. The overall mean annual mortality
rate for the 4 years of accurate data was 23.8%. Interestingly, the average
for adults (24.0%) was virtually identical to that for immatures (23.1%),
suggesting that the specific mortality factors involved may not have
been ones that were especially age dependent.
Verner (1978) calculated maximum permissible combinations of
adult and immature mortality rates for population stability of condors
based on various productivity assumptions. If we assume that (1) age
of first breeding is 6 years, (2) 80% of adults are members of breeding
pairs, (3) nesting success is roughly 50% per attempt, 50% of nesting
TABLE II
Timing of Disappearance of Photo documented Wild California Condors"
Bird Date last observed
WGI August 10, 1982

UN3 September 11, 1983
CCM October 27, 1984
PPF October 27, 1984
CVF November 6, 1984
PCB November 15,1983
SSM November 17, 1984
BOS November 23,1983 (dies of cyanide poisoning on this date)
SBF January 18, 1986 (dies of lead poisoning on this date, but
poisoned by late November 1985)
CVM January 22, 1985
SMA March 15, 1982
Iel March 21,1984 (dies of lead poisoning on this date,
presumably poisoned earlier)
BFE April 10, 1985 (dies of lead poisoning on this date, but
apparently poisoned by late February 1985)
UN2 April 15, 1982
"Une apparently additional adult (not photo-documented); a mateo! PPF, disappeared after Mav 31,
1982.
failures occur early enough to allow renesting, and annual nesting oc-
curs only after early fledging of young (or failure), it is possible to
estimate from Verner's Table 7 that the condor population could 110t
sustain itself with mortality greater than about 9% for adults and 11 (Yo
for immatures, or 7% for adults and 15% for immatures. As the above
assumptions represent our best estimates of the natural productivity
capacities of the species, based on recent data, it appears that the recent
mortality rate has greatly exceeded the maximum allowable for pop-
ulation stability. There can be little doubt that the primary problem of
the species, at least in recent years, has been excessive mortality.
The data on seasonal timing of losses of condors from the wild
population (Table II) indicate that almost no recent losses have occurred
during the warmer months of the year. This effect is consistent with a
number of possible causes of mortality, including weather-related star-
vation, disease, or accidents, as well as shooting and lead poisoning.
But it is not consistent with 1080 poisoning, as the distribution of 1080
to control ground squirrels often takes place in the summer. The absence
of age dependence in mortality rates seems more consistent with poi-
soning than it does with shooting, starvation, or accidents.
As for hard evidence of what specific mortality factors have been
causing the decline, only four free-flying condors were found dead
during the modern program (although at least 15 birds disappeared
since early 1982, and presumably others perished in 1980 and 1981).
All four documented cases were found between late 1983 and early
1986; two were found through radiotelemetry. Of the other birds dis-
appearing, only one was radioed, but both of the bird's transmitters
failed at the time of the its disappearance, so the bird was not recovered.
This fact is in itself suggestive, but hardly proof, that the bird may have
been a victim of human molestation, perhaps shooting.
It is especially interesting to note that from 1982 onward, only 3
of 9 radioed birds died, while 12 of 15 unradioed birds disappeared.
Although the exposure times of the radioed and unradioed birds were
not strictly comparable, these proportions are highly significantly dif-
ferent (p < 0.01), which might at first seem to suggest that radios in
some obscure way might be protecting the birds from mortality. This
difference was especially striking over the winter of 1984-1985, when
only 1 of 8 radioed birds perished while 5 of 7 unradioed birds died
(p < 0.01). We are reluctant to conclude that the radios in any way
protected condors, but the data certainly give no force to conclusions
that radios increased mortality rates. We are inclined to attribute the
high degree of statistical significance here to a bizarre stroke of chance-
and actually a very unfortunate stroke in the sense of lost opportunities
to gain information on causes of mortality.
Nevertheless, the four birds found dead or dying were all given
extremely thorough postmortem examinations by Marilyn Anderson,
pathologist at the San Diego Zoo, and by the contaminants staff of the
Patuxent Wildlife Research Center. Causes of death were determined
for all four. The results were intriguing. Three of the four birds died of
lead poisoning, and of these, two still had lead fragments in their diges-
tive tracts (Janssen et 01., 1986). The fourth bird died of cyanide poi-
soning from an M-44 trap ("coyote getter") set for coyotes (Canis 10-
trans). In addition, one of the three birds dying of lead poisoning had
eight pellets of shot scattered through her tissues from a previous shoot-
ing incident (these pellets were not in themselves the source of the lead
poisoning or cause of death).
Although this was not a large sample of mortalities from which to
generalize, we believe the results are powerfully suggestive that even
though lead poisoning had not ever been confirmed as a cause of death
of the species previously, it has very likely been a major source of
mortality. Lead poisoning of condors had never been considered by
early researchers, though it was a problem we had anticipated as a
possibly important threat (Snyder, 1983; Elveru, 1983) because of the
CONDOR IlIOLOC;Y AND CONSERVA nON 205
earlier deaths of several cathartid vultures in captivity that had inad-

vertently swallowed lead fragments (Decker et aI., 1979; Locke et aI.,
1969), including one Andean Condor at Patuxent. With the amount of
shooting of game and predators that characterizes southern California,
exposure of California Condors to the threat of lead in carcasses seemed
inescapable.
Two of the three condors dying of lead poisoning were recovered
through radiotelemetry. If radiotelemetry had done nothing else for the
program than this, its use would have been fully justified, for there is
virtually no chance that these particular birds would have been found
otherwise, considering their obscure locations. The third (unradioed)
bird dying of lead poisoning was recovered only by great good fortune,
as it too was in a remote location far from roads or habitations. A rancher
in Tulare County encountered this bird by chance on cattle patrol. Thus,
the locations in which these birds were recovered give added support
to the a priori arguments made earlier that in the absence of radiote-
lemetry one would be unlikely to recover birds dying of slow-acting
poisons and that a list of birds found dead, such as that given in Wilbur
(1978), could very easily be highly biased.
To be rigorous, the three recent cases of lead poisoning are not
enough to document exactly how much of a problem lead poisoning
has been for the species. But any way one looks at the issue, it is difficult
to escape the conclusion that lead poisoning very likely has been a
major problem, especially when three additional points are considered.
First, 5 of 14 wild California Condors blood-sampled between 1980 and
1986 carried elevated lead concentrations (Wiemeyer et aI., 1988). Sec-
ond, a condor found shot in Kern County in 1976 had an elevated lead
concentration in bone tissue, apparently stemming from an earlier di-
etary exposure (Wiemeyer et aI., 1983). Third, a study of lead concen-
trations in Turkey Vultures (Cathartes aura) in southern California con-
ducted by the CDFG in 1981 revealed elevated lead concentrations in
about one half the individuals (Wiemeyer et aI., 1986). Taken together
with the three conclusively documented cases of condor lead poisoning,
these facts strongly suggest that exposure of condors to lead has been
a reasonably frequent occurrence. Furthermore, the small size of the
lead fragments found in condors killed by lead suggests a very high
sensitivity to such poisoning.
From what sources is lead contamination most likely? The sorts of
food eaten by condors include a variety of domestic vertebrates, es-
pecially cattle and sheep, which are unlikely to be shot, although cattle
were commonly shot for hides in the nineteenth century (Dana, 1840).
Among wild vertebrates often eaten by condors, however, are three
species that are commonly shot-mule deer (Odocoileus hemionus),

coyotes, and ground squirrels-the first as a game animal; the second
as a target of ranchers, recreational shooters ("plinkers")' and predator
antagonists; and the third as a target mainly of plinkers. In addition,
fur trappers in the back country of southern California generally use
leg-hold traps and dispatch trapped animals, primarily gray foxes (Uro-
cyon cinereoargentatus) and bobcats (Lynx rufus), by shooting, leaving
the carcasses of skinned animals for scavengers.
All the above species are commonly shot with lead bullets, rather
than lead shot. Indeed, in one of the three condors dying of lead poi-
soning, it was possible to recover the lead fragment from its digestive
tract and it was quite clearly a sliver, most likely a fragment produced
by a bullet striking bone. Which of the above sources might be the most
significant source of contamination is unknown, but one should not
conclude from the fact that hunter-shot deer are normally removed from
the wild by the hunters that it is unlikely that contaminated deer re-
mains might be a major threat. Not all deer killed by hunters are re-
covered, and in fact we have observed condors feeding on such kills.
Furthermore, hunter-shot deer are normally gutted in the field, and gut
piles may often contain lead fragments. Condors relish these gut piles
as food.
The cyanide-poisoned condor may have been a freak casualty, as
cyanide traps for coyotes (M-44s) are baited with scent concoctions
rather than carcasses and are tiny, inconspicuous mechanisms. Unless
condors sometimes use olfaction to locate food, it would seem generally
unlikely that they might come into close proximity to these traps. While
evidence is not completely conclusive that condors do not use a sense
of smell to find food, experiments run on this possibility at the Los
Angeles Zoo have been uniformly negative (c. Cox, personal commu-
nication), and we have made no field observations that suggest condors
might find food by this capacity (see also Stager, 1964). Potentially, the
one case of cyanide poisoning was a result of the fact that the govern-
ment trapper in the area had been setting cyanide traps in pairs, one
of which may have killed a coyote, thus providing a carcass to bring
the condor into close proximity to the second, which it may have set
off inadvertently.
The cyanide powder in M-44 traps contains fluorescent particles.
The amount of fluorescence in the mouth of the dead condor and the
absence of fluorescence in the stomach of the bird suggested, at least
tentatively, that the bird had set off the trap itself and was a primary
victim rather than a victim of feeding on a poisoned coyote. If so, it is
unlikely that such poisoning has been a common occurrence. No other
cases of M-44 poisoning of condors are known. Cyanide is a very quick-

acting poison, so animals dying from this cause do not normally get
more than a few meters from the source of poisoning before death.
Thus, if condors had been dying regularly from M-44 traps (either pri-
mary or secondary poisoning) in the past, it is very likely this would
have been known, although not necessarily reported.
One other source of mortality we believe deserves some emphasis
is collisions with overhead objects or wires. Although no recent condor
deaths to collisions have been documented, one was directly observed
in 1965, and Koford found strong evidence for two other cases during
his study. Other recent studies (some utilizing radiotelemetry) have
revealed that collisions are an extremely important source of mortality
for various rap tors , cranes, and waterfowl (Olendorff and Lehman, 1986;
Brown et al., 1987; Faanes, 1987), while European workers have found
high loss rates of European Griffon Vultures (Gyps fulvus) and Ciner-
eous Vultures (Aegypius monachus) to collisions (M. Terrasse and
J. Garz6n, personal communication). As many of the powerlines criss-
crossing the recent range of the condor pass mainly over remote, un-
frequented terrain, it is probable that condors dying of collisions would
be rarely recovered. The high mortality rates of other large and relatively
unmaneuverable birds to this sort of threat suggest that it may also be
of considerable importance to condors.
In summary, our best judgment, on the basis of obviously incom-
plete information, is that the principal causes of the excessive mortality
of California Condors in recent years may have been lead poisoning,
shooting, and collisions, not necessarily in that order, although this
would be our best guess at their relative importance. By offering this
judgment, we do not mean to imply that other mortality sources have
been negligible, but we do mean to suggest that future introductions of
captive condors to the wild are likely to succeed only in areas in which
at least these problems are under effective control. Shooting and lead
poisoning are closely related problems, in most respects sharing a com-
mon solution. The difficulties in countering these threats in practice
are considered in Section 4.2.
2.6.4. Habitat Considerations

The primary habitat needs of the California Condor can be con-
veniently divided into nesting area and foraging area requirements.
Nearly all condor nests have been caves in cliffs, although there have
been two known nests in cavities of giant sequoias (Snyder et al., 1986).
These nest sites have all been located in a band of mountainous terrain
distinct from the principal foraging range in the foothills of the San
Joaquin Valley (See Fig. 1), and we emphasize that no confirmed nests
have ever been found in cliff areas within the foraging range itself.
Although on energetic grounds it might seem advantageous to nest as
close to a food supply as possible, essentially all recent condor pairs
have commuted about 30 km one way from nests to their food supply.
Condors have not foraged to any significant extent in nesting areas
themselves presumably because of the dense chaparral characterizing
most nesting areas and low availability of carcasses in this habitat type.
The reasons why pairs have not nested in apparently suitable caves
in the foraging range are not surely known, and could relate to a variety
of factors. One factor we find especially intriguing is the high density
of natural enemies found there. Both Common Ravens and especially
Golden Eagles are much more abundant in the principal foraging range
than in the condor nesting areas, and it is questionable that condors
could nest successfully in the foraging range because of this. Golden
Eagles, which we have twice documented in attempts to take nestling
condors at their nest entrances (both cases thwarted by adult condors),
are characteristic birds of open grassland habitats and are seen only
infrequently in the central mountains where condors nest. And while
ravens now nest commonly in the central mountains, there are some
indications that they may have increased there in recent decades, pos-
sibly in response to increased food supplies in the form of road-killed
vertebrates and garbage dumps in the region.
It is interesting to note that while condors have not nested in cliffs
in the principal foraging range, Turkey Vultures have. Conversely, Tur-
key Vultures have not commonly nested in the central mountains. It is
also interesting to note that neither of the Turkey Vulture nestlings we
radioed in the San Joaquin Valley foothills in 1981 survived for very
long. One was indeed a victim of a Golden Eagle, the other disappeared
to unknown causes at about the time of fledging. Possibly, Turkey Vul-
tures of this region do not have the option of nesting at substantial
distances from the San Joaquin Valley because of time and energy limits
to how far they can forage from nesting areas. They may have no choice
but to nest in regions of high predator density.
Condors, with their greater overall speeds in flight, can normally
get to foraging grounds from their nest sites in flights of less than an
hour, and commonly remain on the foraging grounds for periods of one
to three days before returning to their nests. Thus the time and energy
spent commuting between nests and foraging grounds appear to be a
relatively minor fraction of their foraging expenditures.
Whatever the cause may be, the fact that condors have not been
documented nesting in the San Joaquin Valley foothills and the fact
that extremely high densities of Golden Eagles occur year-round in this
habitat have important implications for choice of release areas of cap-
tive California Condors in the future, a subject we return to in Section
4.2.
Within the nesting areas, the condors of recent decades have had
an abundance of good potential nest sites to choose from, and it does
not appear that nest sites have been a significant limiting factor, al-
though condors have sometimes chosen suboptimal sites nonetheless
(Snyder et al., 1986). The nest sites used in recent years have all been
well protected from human disturbance simply because of the diffi-
culties in moving through dense chaparral. There has been no pressing
need to place these nests under official sanctuary status.
Thus, although the Sespe Sanctuary has hosted only a single pair
in recent years, and although we have obtained legal access closures
to only two nests elsewhere, in 6 years of virtually constant daylight
coverage of almost all nests from distant blinds we have seen human
intruders come close to only two nests (both protected by sanctuary
status). A lost troop of boy scouts hiked within a few hundred meters
of one site, and several deer poachers came close to another. In neither
case did the intruders cause any detectable disturbance to the birds,
nor were they apparently aware of the nests.
Furthermore, it appears that the intrinsic protection to nesting areas
provided by dense vegetation has been increasing significantly in recent
decades, as the Forest Service has abandoned maintenance of many
back-country roads and trails that were open, for example, in Koford's
time. We have been obliged to spend many long days cutting access
routes to lookouts and blinds just to be able to study the last pairs,
something that casual hikers or poachers would be extremely unlikely
to do. Despite the proximity to Los Angeles and other population cen-
ters, the last nesting areas of the condor have been almost as wild and
inaccessible as they could be, and the mortality and disturbance threats
to the birds in these areas appear to have been very low.
The foraging areas in the San Joaquin Valley foothills have been
another situation entirely. Here the habitat is open or semiopen grass-
land, and the deer, coyotes, and ground squirrels so attractive to hunt-
ers, plinkers, and varmint shooters are abundant. Furthermore, unlike
the chaparral nesting regions, which are almost 100% federally owned
national forests, the foraging areas are almost 100% privately owned
ranches and are used primarily for livestock grazing. Many ranchers
also derive a substantial portion of their income from leasing out hunt-
ing rights, and poaching is an enormous problem everywhere. In fact,
estimates by the CDFG indicate that most deer shot in the region are
taken illegally. Many ranchers still practice coyote control (by shooting
or poisoning), and many still practice 1080 poisoning of ground squir-
rels.
The foraging range of the remnant population has been vast and,
although there have been some losses of this range to housing devel-
opments and other uses, it is substantially the same range today that
it was in Koford's day and is still used largely for the same purposes
(Studer, 1983). We have made no observations that suggest condors
may have had difficulty finding food. Carcasses have been widespread
and common, and there have been no obvious signs of food stress, such
as starving chicks at nests, failures of pairs to attempt breeding, or an
excessive eagerness of birds to come in to artificially provided carcasses.
Thus, there have been no clear indications that the recent condor
population has been suffering from any shortage of habitat per se, either
on the foraging or on nesting grounds, although the hazards of the
foraging grounds have apparently been the major problem faced by the
species. Essentially all recent mortality of condors has been associated
with the foraging regions.
2.6.5. Formation of a Captive Flock

The creation of a captive flock of condors was delayed by a number
of forces, primarily political in nature. It was not until the demonstra-
tion of replacement clutching in the wild population in 1982, and the
clear evidence for a very low wild population revealed by photocen-
susing efforts in that same year that efforts to take captives began in
earnest. If the process had been delayed much longer, the basically
optimistic prospects that still exist for the species presumably would
have disappeared during the catastrophic population crash of 1984-1985.
Until late 1982, state permission to take captives, other than birds
brought in under emergency situations, was limited to finding a mate
for the only bird in captivity, Topatopa. The candidate birds were lim-
ited to nonbreeding adult females or immature females. Unfortunately,
the breeding status of adult females could not even be established con-
clusively without first capturing birds, sexing them, releasing them
(hopefully marked), and then observing them through a breeding sea-
son. If a female proved to be unpaired, then and only then could it be
brought into captivity, assuming it could be recaptured. These hurdles
effectively ensured that no adult female would be taken during the first
years of the program, especially considering the relative rarity of non-
breeding adult females (something that was unknown at that time).
The alternative of trapping an immature, sexing it before release,

and retaining it if it proved to be female was much more likely to yield
results, but offered the disadvantage that it required years of waiting
for the bird's maturation before any reproduction might be possible in
captivity. In any event, a captive population composed of a single pair
offered little potential for salvation of the species.
Neither of the first two immature birds trapped as potential mates
for Topatopa in 1982 were females. One male was released with radio-
transmitters to initiate the telemetry program; the other was retained
as a captive, despite its sex, because of worrisome health defects (low
weight and a chronic gaping problem). Furthermore, a nestling brought
into captivity in late 1982, when one of its parents disappeared, also
proved to be a male. For some, the taking of three males in a row was
objectionable, but by 1984 females exceeded males in captivity. Being
too restrictive about the sex of birds taken in the initial stages of forming
a captive flock does little except delay the whole procedure.
Fortunately, once taking of eggs was started in 1983, sex restrictions
had to be dropped because there was no way to sex eggs before hatching.
Now the females came in rapidly. In fact of the first 10 condors hatched
successfully in captivity 9 were female (a result differing significantly
from chance, assuming a 1: 1 sex ratio might be normal). The bias
toward females was not brought back to near-equilibrium until the last
wild male was captured in 1987.
In 1983, permission to bring eggs into captivity was limited to first-
laid eggs of all pairs. First eggs were taken and successfully hatched
from three pairs, while the nest of a fourth pair was not found early
enough to allow an egg pickup. Two of the three pairs from which eggs
were taken recycled with second eggs. However, one of the two was
the pair in which the male and female fought over incubation rights
and, since their attentiveness to the second egg was extremely poor,
we also took this egg into captivity on an emergency basis. Although
candling of this egg revealed severe degeneration of embryonic blood
vessels, the egg recovered and ultimately produced a viable chick (Ris-
ser,1983).
The other pair producing a replacement egg in 1983 immediately
lost it to apparent raven predation but then surprisingly proceeded to
lay a third egg 1 month later. This egg produced a viable chick which,
after considerable debate, was also brought into captivity. To have al-
lowed it to fledge naturally would have meant the pair almost certainly
would not have bred the following year. The debate over the fate of
this chick was one of the major issues of the recent program; we consider
the arguments for and against in more detail in Section 3.4.
With the demonstration of triple clutching in 1983, plans for 1984

called for taking both first and second eggs from active pairs. Five active
pairs were found in 1984, but eggs were taken from only four, as the
fifth was nesting in a giant sequoia tree cavity 30 m above the ground,
and there were formidable practical problems in reaching the site. The
chick from this nest, however, was later taken into captivity close to
fledging. Of the four pairs from which eggs were taken, three laid second
eggs that were also taken, and one produced a third egg. When this
third egg was laid in a precarious site only 3 m from an active raven
nest, a decision was made to bring it into artificial incubation as well,
as it had virtually no chance for survival. (The ravens were attempting
to grab it at every opportunity, and this was again the condor pair that
fought over incubation rights, often leaving their eggs unattended for
long periods.)
Only one breeding pair survived into 1985; it produced three eggs,
the third pair to triple clutch. All eggs were incubated in captivity. The
female of this pair was lost to lead poisoning during the winter of
1985-1986, but at the same time 3 new pair bond formed between the
other female in the wild and one of the remaining unattached males.
This new pair laid two eggs in 1986, but only one was incubated in
captivity. The other, a very thin-shelled egg, was crushed before it could
be taken.
Overall, 16 eggs were artificially incubated between 1983 and 1986,
primarily by Cyndi Kuehler of the San Diego Zoo (Kuehler and Witman,
1988). Of these, 13 (81%) hatched and produced surviving young, a
fledging success close to double the normal performance of the wild
population. With the increased fledging success produced by artificial
incubation and the increased numbers of eggs produced by multiple
clutching, the population produced six surviving young in 1983 and
seven surviving young in 1984 (including nestlings raised in the wild),
as compared with an average of two young per year in 1980, 1981, and
1982-a remarkably strong increase in view of the overall population
decline through this period. The population crash of 1984-1985 spelled
the end of massive reproductive increases through multiple clutching
and artificial incubation.
Of the three eggs that did not produce surviving young in captivity,
one experienced early death of the embryo, one hatched but the chick
was grossly abnormal physically and died during hatching, and the
third produced a chick that died of a yolk sac infection shortly after
hatching. It is doubtful that the viability of any of these eggs would
have been any better had they been left in the wild.
In addition to the 13 birds taken captive as eggs, four individuals
CONDOR BIOLOCY AND CONSERVATION 213
TABLE III
Makeup of California Condor Captive Population: 1988
Age Year taken

Bird Sex (years) c.aptive Family line (parentage)
CeF F 14 (min) 1985 CC (parents unknown)

REC M 8 1987 CC (son of CCF and CCM)"
Sisquoc M 5 1983 CC (son of CCF and CCM)
Sespe F 5 1983 CC (daughter of CCF and CCM)
Pim F 4 1984 CC (daughter of CCF and CCM)
Inaja F 4 1984 CC (daughter of CCF and CCM)
Pismo F 4 1984 CC (daughter of CCF and CCM)
SSF F 14 (min) 1986 SS (parents unknown)
Xolxol M {j 1982 SS (son of SSF and SSM)
Tecuya F 5 1983 SS (daughter of SSF and SSM)
Cachuma F 5 1983 SS (daughter of SSF and SSM)
Anyapa F 4 1984 SS (daughter of SSF and SSM)
Squapuni F 4 1984 55 (daughter of SSF and SSM)
Nojoqui M 2 ]986 SS/CC (son of SSF and REC)
SBM rvI 14 (min) 198{j SB (parents unknown)
Almiyi F 5 1983 SB (daughter of SBF and SBM)
Ojai F 4 1984 SB (daughter of SBF and SBM)
Kawl:ah M 3 1985 5B (son of SBF and SBM)
Malibu F 3 1985 5B (daughter of SBF and SBM)
Paxa M 7 1982 CV (son of CVF and CVM)"
Cuyama M 5 1983 CV (son of CVF and CVM)
SMM M 12 (min) 1986 SM (parents unknown)
Sequoia M 4 1984 SM/PP (son of SMM and PPF)
HIW M 8 1985 HW (parents unknown)
UN1 F 12 (min) 1985 UN (parents unknown)
Molloko 0 1988 HW/UN (progeny of HIW and
UN1)
PCA M 12 (min) 1986 PC (parents unknown)
Topatopa M 22 1967 MC (parents unknown)
"Parentage of REC and Paxa assigned from field behavioral data.
were taken as nestlings between 1982 and 1984, one was trapped as a
yearling in 1982, and eight were trapped as free-flying adults and sub-
adults in the last two years of the field program after an enormous
amount of controversy. Table III presents the specifics on the birds in
captivity. With 13 males, 14 females, and one as yet unsexed, captive-
produced chick of 1988, the sex ratio could not be more favorable, but
most birds are still immature. Clearly some family lines are much better
represented than others, and in fact some of the family lines themselves
may be closely related, so there are grounds for concern as to how
viable the flock may be from a genetic standpoint. The captives are
being paired to promote outbreeding and are divided approximately
equally between specially built breeding facilities at the Los Angeles
and San Diego Zoos.
One point that should be addressed here is whether the establish-
ment of the captive flock was a major cause of the simultaneous decline
of the remnant wild population. With the exception of Topatopa, a
starving wild fledgling of 1967, no captives were taken before 1982, so
the decline of the species prior to that time can hardly be attributed to
this cause. After early 1985, on the other hand, the decline was nearly
100% attributable to this process, consciously and deliberately, as the
consensus was strong by then that the remnant wild flock was inviable.
The period of real interest was from early 1982 to early 1985, during
which there were still sincere hopes that the decline of the wild pop-
ulation might be reversible. During this period, only one condor was
allowed to fledge naturally in the wild, while the wild population
declined from about 23 to 9 individuals.
How many wild condors would there have been in early 1985 if
captives had not been taken? If we assume that the wild population
would have naturally produced young at the same rate in 1983 and
1984 that it did in 1980, 1981, and 1982, then there would have been
five additional birds fledged in the wild: one fledged in 1982, two in
1983, and two in 1984. In addition, since we trapped one yearling for
the captive flock in 1982, he must be added to the total. But the total
of six additional birds has to be adjusted by natural mortality that
presumably would have occurred during the period from 1982 to 1985.
When this is done, the total of six drops to four. Thus, in the absence
of multiple clutching and taking of captives, the expected total wild
population by the spring of 1985 would have been only 13 individuals,
still representing a severe decline from the 23 of early 1982. The taking
of captives during this period accounts for less than one third of the
population decline and therefore cannot be considered the major cause
of decline (see Johnson, 1985).
2.6.6. Summary of Causes of Decline

Data gathered during the modern program leave little doubt that
the major cause of the recent decline has been excessive mortality rather
than reproductive failure and, while it is unlikely that the specific

stresses faced by the species have remained constant through time, there
is no strong evidence for reproductive problems during any period since
the first intensive studies of Koford. Documented reproductive success
remained reasonably strong even through the 1960s, when DDT stress
was at a maximum (Snyder, 1983), although the ratio of immatures to
adults on the October Survey did show a drop during the early 1970s
(see Section 3.2). Wilbur's (1978) assertion that condors largely stopped
breeding during the 1970s is not supported by careful documentation
of inactive pairs at the time and appears to have been largely a con-
sequence of his considering the Sespe Sanctuary to be the major area
for condor breeding and his failure to look extensively for active pairs
elsewhere. Rigorous documentation of lack of breeding is difficult to
obtain and takes many days of steady observation of all possible nesting
areas because visits of condors to nests are often spaced many days
apart. Such determinations cannot normally be made without massive
investments of manpower, and such manpower has only become avail-
able in very recent years. Wilbur quite clearly missed a number of active
pairs during his studies.
A comprehensive accounting of the specific mortality factors re-
sponsible for the decline has been difficult to obtain, and our present
judgments as to what factors have been most important are based on
too few data to be considered definitive. Nevertheless, what data are
available suggest that lead poisoning, wanton shooting, and collisions
have probably all been important problems in recent times. Two of
these problems, shooting and lead poisoning, have presumably been
important since the first western settlers entered the range of the spe-
cies.
In addition, it seems clear that historically many condors were lost
to a number of stresses that now are apparently much reduced in im-
portance, namely predator-poisoning campaigns using strychnine and
cyanide baits, egg collecting, and museum collecting of adults and
immatures. However, it is reasonable to suppose that replacement
clutching greatly mitigated the impacts of the egg collectors. No good
evidence has yet been assembled that the condor has been suffering
from human disturbance per se, as opposed to mortality factors. Nor
has good evidence yet been obtained of a significant threat from 1080
poisoning of ground squirrels.
Some observers have expressed fears that the condor has been
suffering from loss of habitat. But if one surveys the extent of the recent
range of the species by air, one very quickly comes to appreciate just
how enormous and basically untouched by modern developments it is
and to realize that completely similar habitat, formerly occupied by

condors, extends beyond the limits of the known range in all directions.
That the condor's primary problems might be those of loss of either
nesting or foraging habitat is simply not reasonable, although the spe-
cific hazards that have been present within the habitats used by the
species, especially on the foraging grounds, appear to have been major
problems. Controlling these hazards, not habitat preservation per se,
has been and will be the challenge.
The lesson that habitat loss has been responsible for the endan-
germent of many species has been learned too well. While it is a truism
that all species must have adequate amounts of the habitats to which
they are adapted, it does not follow that all endangered species are
stressed by habitat limitations. Some endangered species, among them
apparently the condor, are in trouble because of much more specific
stresses, and no matter how much habitat is acquired for these species,
they will still decline if the specific stress factors are not brought under
control. For the condor, habitat preservation appears to be one of the
least pressing priorities in the short term, though we do not wish to
minimize its importance in the long term.
Because of these considerations, the documentation of which spe-
cific areas condors have been using most intensively does not in itself
indicate which areas are most valuable for the species in the future, a
point that has often been misunderstood. In fact, since the species has
been declining so rapidly, one could argue that certain of the high use
areas may actually be the most risky areas for the condor to occupy.
Unless the specific threats that characterize these areas can be fully
controlled, they may represent "black holes" for condors indefinitely.
Extensive documentation of which areas have received intensive
use by which condors has now been achieved by on-the-ground ob-
servations, photoidentifications of birds, and radiotelemetry. What this
information should be used for in terms of habitat preservation or ac-
quisition efforts is a much more complicated and unclear issue that we
leave to the second half of this paper, as it is primarily a political rather
than a biological question.
3. HISTORY OF CONDOR CONSERVATION
Before plunging deep into the quagmire of condor conservation,

we must assure the reader that despite the personal frustrations we
experienced while in the condor program, we actually hold a fairly
positive overall viewpoint concerning the outcome of the political
CONDOR BIOLOGY AND CONSERVA nON 217
machinations that have characterized nearly five decades of condor

conservation efforts. Despite many bitter battles, considerable progress
has been made, and the primary problems that have characterized con-
servation efforts have been a shortage of good information on exactly
what the causes of the species' decline have been and basic disagree-
ments as to what constitute effective and permissible ways of gaining
that information. Although for many years condor conservation efforts
have proceeded in relatively unproductive directions, prospects for
ultimate survival of the species still remain reasonably good. And while
it has often seemed that certain organizations and individuals have
been mainly concerned with fitting the condor into preconceived con-
ceptual frameworks and with using the species to achieve goals unre-
lated to its own conservation, it has been clear that underlying the
concerns of nearly everyone involved with the condor has been a sin-
cere desire to see the species survive and prosper. When good objective
data on the realities of condor biology have finally been in hand, con-
troversies have mostly evaporated. Politics have eventually come to be
consistent with biology, and the real struggle has been to get the biology
straight when politics have so often obstructed desperately needed re-
search and conservation endeavors.
The following sections concentrate on certain key concepts and
controversies that have been especially important in the history of con-
dor conservation. Our objective is to examine why these concepts and
controversies have developed and what effects they have had on sub-
sequent events. We present our own point of view on these matters, to
be sure, but we hope we are also successful in presenting other points
of view in enough detail that the reader may come to understand why
some controversies have endured as long as they have. In this discus-
sion, we depart at times from straight biology and venture into the more
speculative and subjective terrain of values and beliefs. We believe
there is no other way to make sense out of what has transpired.
3.1. The Condor as a Symbol of Wilderness: The Controversies

of the 1940s and 1950s
One of the most important shifts in human perceptions of the con-
dor occurred during the Koford era, when an image emerged of the
species as an incredibly shy and sensitive creature, almost completely
intolerant of the presence of man. This was a surprising development,
because there are no indications from Koford's field notes that he held
this viewpoint at the time he conducted his research. Koford was in
and out of active nest caves with a frequency that now seems quite
remarkable. For example, he visited his nest No.5 a total of 14 times

during the incubation period in 1941, yet took hardly any data during
these visits. It is difficult to deduce why such frequent close interactions
with nesting condors may have been necessary but, on the other hand,
we do not believe that there is clear evidence that these nest visits were
in a very significant way harmful to the birds. The major puzzle after
reading these notes is to understand how the image of the condor as a
creature so behaviorally sensitive to man ever arose, a creature likely
to desert its nest should a man so much as "expose himself" within a
few hundred meters (for an extreme development of this point of view,
see McMillan, 1981). Our own perceptions of the species' attitudes
toward mankind differ markedly from this image and instead are close
to those projected by Finley so many years ago.
Although one can only speculate on what caused the change in
perceptions, one wonders whether Koford, late in his study, began to
have misgivings about the unrestrained way in which he had conducted
his early research, a feeling triggered perhaps by the failure of an egg
to hatch at nest No.5 in 1941 or by the apparent breakage of a nestling's
wing during handling in 1939, or by the failure (to unknown causes)
of a heavily visited nest of 1945. However, it must be noted that Koford
still continued to enter nests freely as late as 1946, the last year of his
field studies.
Could the efforts to secure a Sespe Sanctuary during the late 1940s
and early 1950s have had anything to do with the changing perceptions
of the species? The Sespe Sanctuary was first established as a 14,000-
ha preserve in the Los Padres National Forest in 1946, was later enlarged
to 21,450 ha and partially withdrawn from mineral leasing in 1951, and
was finally withdrawn entirely from mineral leasing in 1970. During
this period, there was considerable discussion regarding need for the
sanctuary and the degree to which it should be closed to human entry.
A review of the process of securing this sanctuary generates a number
of questions. Did advocates of the sanctuary find it more advantageous
to present an image of the condor as a creature tolerant of man's pres-
ence or to emphasize crucial needs of the species for isolation from
man? Was it more effective in the efforts to get a sanctuary to emphasize
low or high estimates of condors left in the wild? Specifically, to what
extent did efforts to secure the sanctuary influence the dropping of
qualifying statements as to numbers of condors as one proceeded from
Koford's dissertation to his published monograph (the monograph oth-
erwise is close to a verbatim repetition of the dissertation). To what
extent, as well, did the new image of the condor as a man-intolerant
species fit in with man's psychological needs for a living symbol of
wilderness-a creature of great rarity, mystery, and incompatibility

with man? We pose these questions not to imply certainty as to what
may have transpired so long ago, but to call attention to a number of
concepts that may plausibly have had some relationship with one an-
other.
One thing that is clear is that sometime during the 1940s and early
1950s, the condor ceased to be an exciting and uncommon, but never-
theless approachable, wildlife species that egg collectors, photogra-
phers, and researchers mingled with relatively freely. It became a sacred
spirit-not in the sense of its bygone religious significance to early
Indian tribes of California, but in a distinctly modern sense as a focus
of wilderness worship. The species took on attributes that it did not
possess previously-attributes that some may have felt quite sincerely
would help ensure its conservation-attributes that at the same time
may have fulfilled very fundamental twentieth century human needs
for a species that might epitomize unknowable pristine nature, a species
totally apart from man, at least modern man.
Perhaps the real condor did not quite fit this symbolic role, but it
was close enough. Without a doubt, its enormous size and striking
appearance were inspiring. Its nesting areas were certainly wild, re-
mote, and spectacular, and its very name sounded a note of mystery
and power. While its basic lack of wariness did not harmonize well
with the overall image, this could be defined away. The fact that the
condor was heavily dependent on domestic livestock and hunter-killed
wildlife for food in some of the most degraded grasslands of the region
was not quite right either. But although these lands were not wilderness,
they were certainly picturesque enough, and what apparently really
counted was the fact that the ranches had been there long enough that
no one remembered what the land looked like before them. If not true
wilderness, they were at least pastoral enough to evoke powerful emo-
tions of nostalgia for a disappearing America that blended with the
appeal of wilderness. Conservation of the condor in the minds of many
became equivalent to trying to hold on to the past, not the distant past
that no one remembered, but a more recent past that included herds of
sheep and cattle and ranching as a way of life. Condor conservation
became a crusade difficult for anyone depressed with the march of
civilization to resist.
In this evolution of perceptions, it has often seemed that the main
goals of condor conservation have become indistinct. The condor "is"
habitat, it has sometimes been said, and from the time of establishment
of the Sespe Sanctuary to the more modern fights for a Sespe-Frazier
Wilderness and for Hudson Ranch, one cannot escape the impression
that for many people involved in condor conservation, preserving hab-

itat and preserving an image of the condor as a paragon of wilderness
have been more important than saving the condor itself. Perhaps these
are more important goals, but we disagree that they are equivalent to,
or even always consonant with, preservation of the condor as a viable
biological species.
Donald D. McLean, an employee of the California Department of
Fish and Game during the Koford era, touched on some of these ques-
tions in a letter to Allan Phillips dated March 14, 1958, in which he
primarily discussed his sighting of a group of 85 condors in the An-
telope Valley north of Neenach in 1942, a sighting mentioned (and
dismissed) by Koford (1953) with a terse, "This is more than my esti-
mate of the total population." Excerpts from McLean's letter follow:
Perhaps when you are told to slant your findings to fit your sponsor, you
have to do it or lose your funds!? Of course the whole condor study program
was set up as a propaganda scheme to get the condor sancutary .... Birds
on P 145 [of Koford's monograph] were feeding on a large dead steer that
had died of anthrax or black-leg, one of a number that had died there. Some
25 or 30 condors were around the relatively fresh carcass. Most of the
remainder were standing on the dry grass slopes of two small knolls just
above the dead animal. Some were circling low over the area and brought
our attention to the spot. They were "counted", not estimated, not only by
me but by my chief at the time [in the Department of Fish and Game], J. S.
Hunter .... Joe was not able to see the group on one of the knolls. I took
16 mm movies of all I could get, but of course I could not get them all in
the picture at one time. Carl [Koford] could never seem to arrange to see
these films. So far as I know the picture is still in the possession of H. M.
Bourland and is incorporated [in] two 400-ft reels of condor film which we
worked on together ....
Now here is something I have rarely mentioned to anyone: about 2
hours and 80 air miles later, on the same day, we were travelling up the
western side of the Carrizo Plains in San Luis Obispo County and saw 37
condors feeding on and standing about several dead sheep. I don't say that
some of the Antelope Valley condors could not have beaten us up to the
Carizzo Plains, but I doubt that well fed condors would have crossed the
Tehachapi Mountains and headed that far north to take on another feed of
sheep, with still plenty of beef available.
I can't be convinced by anyone that there are any less than 50 breeding
pairs of condors .... I know of a considerable number of nesting areas not
mentioned in any publication and I'm not about to reveal them, that is the
exact areas.
Carl spent by far the largest part of his time in the one area, which had
been pre-chosen as the proposed condor sanctuary.
Nests in the Havilah and Piute ranges south of Kernville and the eastern
Tehachapis east of Monolith, as well as those on the Hurricane Deck, east
of Los Olivos in Santa Barbara County and the Caliente Range on the west
side of the Carrizo Plains in San Luis Obispo County, have failed to make
the printed page, of late, at least. I find no mention of any nests in the Pim
Gorge either, one of them can be walked to by a lady in high heels, as it is
in a round jug-necked hole on a smooth solid rock slope of about 20 degree
slope.
Condors are not about to become extinct, providing a good portion of
them nest elsewhere than in the "sanctuary." No sheep or cattle there.
Although we have been unable to locate the McLean film, Fred

Sibley (personal communication) was able to see it in early 1967 and
confirms that it scans over many condors, although, as McLean indi-
cated, it is not possible to count more than 25 or so in view at once.
As to the accuracy of other statements made by McLean in his letter,
we do not know whether condors once nested in all the locations he
mentioned, although condors definitely have nested in some of these
areas and most are reasonable possibilities. We have attempted to locate
his site east of Monolith, as did Fred Sibley, but without success, though
we would stop short of saying that condors never nested there. It is too
easy to miss old condor nests. On other subjects, McLean (now de-
ceased) has been a source of mixed reliability. His information on old
Peregrine (Falco peregrinus) nest sites has been relatively poor (L. Kiff,
personal communication), although his information on old Pileated
Woodpecker (Dryocopus pileatus) territories has been impressively ac-
curate (G. Christman, via Fred Sibley, personal communication).
Regardless of whether or not one wants to accept McLean's condor
sighting of 1942, it appears likely that this sighting became the basis
for an unofficial estimate of 150 or more condors left in the wild by
the CDFG (see McMillan, 1953), an estimate that accords well with our
own independent estimate of the condor population at that time, and
an estimate that had relevance not only for discussions over establish-
ment of the Sespe Sanctuary but also for a much more tempestuous
controversy that arose during the same period-the permit granted the
San Diego Zoo by the California Fish and Game Commission (CFGC)
to capture two wild condors for captive breeding.
The early request of the San Diego Zoo to initiate captive breeding
of condors is a classic example of the failure of an idea that was ahead
of its time. Belle Benchley and K. C. Lint of the San Diego Zoo had had
great success during the 1940s in breeding Andean Condors in captivity.
This success included the routine laying of more than one egg per year
by their breeding pair (replacement clutching). As a natural extension
of this success Benchley approached the CDFG in 1949 with a proposal
to take a pair of California Condors, not just to breed them in captivity,
but to serve also as a source of birds to release to the wild in an effort
to bolster the wild population.
The CDFG was receptive to the idea of captive breeding, as it be-

lieved that removal of two birds represented no significant threat to the
wild population. With the support of the CDFG, the CFGC readily ap-
proved the permit request, although it expressly forbade releases of
progeny to the wild in apparent fear that this might introduce avian
diseases from captivity into the wild.
Then the troubles began. Alden Miller, Carl Koford, John Baker of
National Audubon, and Ian McMillan all linked arms to protest the
action, publishing a number of articles denouncing it as possibly the
difference between survival and decline of the wild population. Miller
(1953) pointed out the possibility that trapping two adults could disrupt
reproduction of two pairs in the wild, or even more if more than two
birds had to be trapped to get a heterosexual pair, and how this, par-
aphrasing calculations of Koford, might lead to failure of as much as
60% of the five pairs normally successful in the population during any
year! As Miller summed up the situation:
The danger in trapping and removing adults lies then in tipping the balance
in this precariously situated species. It is very difficult to say, scientifically,
which straw will break the camel's back, but cutting significantly into the
annual reproduction of a threatened species seems distinctly dangerous.
Even if the disruption from trapping were not disastrous, several years
would be required for the species to recover its former numbers after the
adults were taken.
This dire warning took no note of intentions of the San Diego Zoo to
trap immatures if at all possible, and was of course a worst case of all
possible worst cases, based on calculations that today seem remarkably
naive and conservative in their assessment of reproductive capacities
of the species. That anyone could seriously suggest that the taking of
two adults from a population of 60 birds (it was probably more like
150 birds) might be a major factor in survival of the population is
astounding.
Nevertheless, we do not question that Miller and his allies were
acting in a rational manner. What they feared most of all, we believe,
was that captive breeding would become a substitute for efforts to save
the wild population, and might ultimately lead to opening the Sespe
Sanctuary to development. Furthermore, we have little doubt that for
some people the possibility of opening the sanctuary to oil exploration
and hunting would indeed be an underlying motive for why they might
have supported captive breeding, though it is clearly not the way the
San Diego Zoo viewed the situation. The modern concept of captive
breeding working in concert with efforts to save wild populations was
not yet born and although Belle Benchley was trying valiantly to get
this idea started with condors, it is really no surprise that it was greeted
with deep suspicion and hostility. Zoos had no record of participation
in such efforts to point to at that time, and such a role for zoos was
then totally contrary to popular perceptions. Ironically, today it is the
San Diego Zoo, together with the Los Angeles Zoo, that bears the over-
whelming responsibility for survival of this species under much more
difficult odds than existed during the early 1950s.
The first attempt to obtain wild condors for captive breeding ended
when Ian McMillan and other opponents went over the heads of the
Department and Commission and successfully lobbied the California
Legislature to specifically prohibit any taking of wild condors. Although
the San Diego Zoo carried out trapping efforts for condors up to the
time this legislation went into effect in early 1954, they were unsuc-
cessful in capturing any birds.
The winners of the early battles to establish the Sespe Sanctuary
and to stop initiation of captive breeding of condors were hands down
the NAS, Miller, Koford, the McMillans and their supporters. They
were also winners of a more subtle and ultimately much more important
campaign; the condor was now enshrined as a species too sensitive to
even approach safely, too sensitive to study closely, too delicately bal-
anced above extinction that initiated captive breeding could be without
endangering the population. The condor had become untouchable. Had
the Sespe Sanctuary proven sufficient to stop the decline, this latter
victory of perspectives would not have been especially harmful. But
the Sespe Sanctuary, and in fact the whole sanctuary approach, proved
inadequate. And now the perceptions of the species that went along
with this approach became an oppressive curse to true conservation of
the species, a curse that endured for more than 30 years, totally inhib-
iting needed research at times and most unfortunately preventing even
tentative movements toward captive breeding that might well have
made the recent history of conservation efforts for the species read very
differently.
For those on the fringe of condor conservation efforts, those with
no real personal experience with the species, the perception of it being
an extremely wary and sensitive creature has been a very comfortable,
even attractive idea. Are not rare birds always sensitive and wary? And
to have researchers such as Koford, Miller, and the McMillans affirming
this perception has for many observers put it beyond question.
Nevertheless, condors have continued to have a contrary habit of
flying in curiously from a distance to circle low over people's heads,
sitting placidly for frame-filling portraits by hikers armed only with
Instamatic cameras, accepting banana peels and peanut butter sand-
wiches from passers-by, and walking unconcernedly along the shores

of heavily used lakes with waterskiers whizzing along only a few meters
away (these are all documented occurrences). The mental contortions
required to render such incidents consistent with the image of a wary
wild condor have sometimes been awesome.
Eben McMillan (1981) has offered perhaps the most detailed rec-
onciliation of these apparently contradictory concepts:
You know, behaviorists, working with other animals, have established that
there is what is known as a delayed response to disturbance. Photographers
see this a lot. You go in to photograph a bird on a nest, and the bird will
sit right there; you scare it off, and it'll come right back. You're ready to
come back in two days and there's nothing there. This kind of thing happens
again and again. The way the bird behaves when you're there is no indication
at all of what the bird is going to do six, 24, or 48 hours later. Carl [Kofordl
brought this out in his paper on the condor. He told about things he had
seen where the birds would respond to a disturbance, or a pressure, long
after it happened. The birds might be roosting in a particular tree, and a
guy would drive some cattle through or a birdwatcher would come up. And
the birds would sit right there while the cattle went by underneath. Maybe
the guy had seen them for a week coming to that roost, but the next day,
they didn't come back. Not only that, but they never came back at all; they
never came to use that tree again, as a roost. Carl was one of the early
observers of this phenomenon, the delayed response.
Perhaps the nesting birds that disappeared in McMillan's illustra-

tion were victims of nest predation caused by the photographer ex-
posing the nest to view or leaving a scent trail to the nest, and perhaps
his condors would never have come back to roost in that particular
tree, disturbance or no disturbance. (Did anyone, in fact, sit in view of
the tree month after month to see whether condors ever came back?)
Koford actually did not mention any such instance in his monograph
or field notes.
And strangely, the condor pair we observed walking along the
beach of a heavily disturbed lake during the early 1980s did keep com-
ing back week after week, month after month, year after year, sometimes
walking up to within 5 m of us, often not even looking up as they
puttered through debris on the shore, with speedboats roaring by. We
waited patiently for a sign of a delayed response in these birds.
It would be inaccurate to imply that all condors have been as
approachable as the lake pair. This pair evidently had become thor-
oughly habituated to people through frequent contact. As in most bird
species, different individual condors exhibit different thresholds for
response to human approach and, as in many other species, juveniles
tend to be especially approachable. Granted, some individuals, like
individuals of many raptor species, will flush from a nest when a person
is many meters away. But as we learned during egg pickup operations
during the mid-1980s, such wariness is exceptional, and most incu-
bating birds will not leave their nests without very close approach.
Koford found it necessary on one occasion to throw rocks at the cliff
next to a nest to get an adult to appear at the entrance for Pemberton's
photographic efforts. Contrast this with the behavior of most large raptor
species.
Fred Sibley, in his 1967 field notes, recorded an interesting obser-
vation on the absence of long-term effects of human disturbance on a
traditional condor roost in northern Kern County:
A roosting locality on Breckenridge Mountain referred to in Koford's notes

was watched for one day and two birds were seen. When Koford first found
this roosting site in 1946 there was considerable human disturbance, and
one would have expected the birds to have moved elsewhere. The morning
I watched there was heavy traffic on a road 200 yards from the roost, mod-
erate activity at the numerous summer homes i-I mile away, a chain saw
going within ~ mile of the roost and one ear-splitting sonic boom which
echoed and reechoed up and down the mountain. Despite all this activity
the birds departed at a "normal" time over an hour after the "disturbance"
activities had reached their plateau.
This roost has continued to receive condor use in more recent years.
In our experience, the condor has been one of the most approach-
able large birds we have ever encountered. This should not be taken
to imply that we believe there are no risks to nest entry and especially
to handling of chicks or to imply that we do not support generous buffer
zones around nests and roosts. We most emphatically do. But the notion
that condors will desert nests and roosts merely because someone walks
nearby is directly contradicted by an immense body of observational
evidence. There are far more wary birds in the wild than the condor
and, as long as this species is not directly molested, it appears to be a
relatively compatible species with man behaviorally. The incredible
wariness of the California Condor is a myth.
In fact, when one closely examines Koford's (1953) voluminous
comments on reactions of condors to disturbance at roosts and nests,
one discovers that he is describing responses that can be seen to a much
more extreme degree in many other familiar species, for example, Red-
tailed Hawks (Buteo jamaicensis). Yet the fact that he emphasized the
potential effects of disturbance so greatly is what really comes across,
and it is this general impression that people have come to remember
and exaggerate.
How crucial then has the Sespe Sanctuary been for survival of the
condor? This is not an easy question to answer, and we must admit we

are basically very pleased that the sanctuary was established and strongly
support its maintenance, as we feel it represents one of the best places
for future efforts to reestablish condors in the wild. But to be perfectly
honest, whether or not the sancutary had been established, we believe
the present status of the species would probably have been about the
same. Most pairs in recent years, and almost surely in Koford's day as
well, have nested outside the sanctuary, and the nesting areas outside
the sanctuary have been almost as well protected as those inside by
their remote locations and by the surrounding brushy terrain. It is dif-
ficult to make a case that the sanctuary has greatly slowed the decline,
when the principal problems of the species have evidently been on the
foraging grounds many kilometers away.
On the other hand, there might well have been more cases of human
molestation of condors in the sanctuary region if a sanctuary had not
been established. Very likely, more oil roads would have been built,
providing access to gunners and curiosity seekers to certain nests. The
fact that we found a spent bullet in the nest litter of one sanctuary site
close to an oil well (Snyder et aI., 1986) was a graphic indication that
even though nesting condors might not greatly fear man, they might
suffer high mortality by nesting close to him.
But in the balance, one could argue that the price that was paid
for the sanctuary, in terms of changed perceptions of the condor (if it
is fair to attribute these changes to the process of acquiring the sanc-
tuary) and in terms of later research being focussed too tightly on this
piece of real estate, haD been a very steep one. Did the end justify the
means?
3.2. Conservation and Controversies of the 1960s

The major advance represented by the study of Miller et a1. (1965)
over that of Koford (1953) was that Miller et a1. were convinced that
the condor population was in rapid decline whereas Koford had be-
lieved it was essentially stable. Nevertheless, the conservation rec-
ommendations of Miller et a1. were almost carbon copies of those of
Koford. Like Koford, they called for federal protection of the condor,
increased education and law enforcement efforts to reduce threats of
shooting and molestation, increased protection from human distur-
bance for nesting and roosting areas, further study of the effects of
poisons (especially 1080) on surrogate species, and a full-time condor
warden to patrol areas of high condor activity. In addition, they called
for an end to coyote control with poisoned carcasses and recommended
closure of some specific condor flyways to shooting, especially the

Sierra Madre ridge in Santa Barbara County and Pine Mountain in
Ventura County. Furthermore, they called for the prohibition of low
overflights of the Sespe Sanctuary by aircraft. But note especially, nei-
ther Koford nor Miller et 01. recommended a stoppage of all shooting
and all 1080 poisoning of rodents in the range of the condor. Then, as
now, such steps would have been politically explosive, and very likely
counterproductive to conservation of the species.
A very large fraction of the above recommendations were ultimately
implemented. The condor was given federal protection under the En-
dangered Species Acts of 1966 and 1973; greatly increased education
on the plight of the species did occur through publication of numerous
magazine articles and books and through innumerable talks and dis-
cussions, especially those conducted by NAS personnel; protection of
the Sespe Sanctuary was enhanced by seasonal firearms closures of
buffer areas and by closure of accessory nesting areas such as the Piru
Gorge; while private inholdings in the Los Padres National Forest, such
as the Green Cabins and Coldwater Canyon nesting areas, the Sespe
Hot Springs area, and the Hi Mountain nesting area were purchased
and given protection. In addition, the Percy Ranch adjacent to the Sespe
Sanctuary was purchased and set up as the Hopper Mountain National
Wildlife Refuge, and a large fraction of the condor nesting range in
Santa Barbara County was set aside as the San Rafael and Dick Smith
Wilderness Areas. Furthermore, a full-time condor warden (John Borne-
man) was appointed by NAS in 1965; the Sierra Madre Ridge Road was
maintained closed to public vehicular traffic; an aircraft prohibition for
the Sespe Sanctuary region was instituted; and an intensive study of
the field effects of 1080 poisoning of ground squirrels was conducted
by the U. S. Fish and Wildlife Service in 1977 (but indicated no clear
threats to raptors or vultures; see Hegdahl et 01., 1979). In addition,
coyote trapping efforts of the Animal Damage Control branch of the
U. S. Fish and Wildlife Service became limited to scent-baited traps.
Good summaries of many of these and other conservation actions are
given in Wilbur (1978) and Jurek (1983).
Despite the many protective steps taken, the decline of the species
continued. For some people, bureaucracy was still to be blamed for
inaction, while the adequacy of the recommendations of Koford and
Miller et 01. was not to be questioned.
In hindsight, the failure of the recommendations of Koford and
Miller et 01. to reverse the decline is not surprising. For even if these
recommendations had been implemented to the 100% satisfaction of
these researchers, even if the whole Los Padres National Forest had
been sealed tight from human entry, even if not a single condor had
been shot since the 1940s, and even if 1080 and strychnine poisoning
had been completely stopped throughout the condor range, the chances
are still very large that the decline of the species would have continued,
and possibly at virtually the same rate as actually occurred. Three out
of four condors found dead in the 1980s were victims of lead poisoning,
very possibly caused by entirely legal and nonmalicious hunting of
wildlife such as deer in areas far from the Los Padres Forest. The rec-
ommendations of Koford and Miller et a1. did not address this threat.
Nor did their recommendations address the threat from collisions with
overhead wires, which is now known to be a severe hazard to large
vultures in general. The recommendations of Koford and Miller et a1.
were very reasonable ones in view of the information they had available,
but their information was far too incomplete to allow development of
fully effective conservation efforts.
The proper response to this failure should have been, and ulti-
mately was, a general recognition that much better data were needed
on the causes of the species' decline, but for some people further re-
search was not only unnecessary but dangerous, and the decline of the
species was still to be attributed to a failure of bureaucracy to save
enough habitat and to stop 1080 poisoning and wanton shooting of
condors.
One of the most unfortunate results of the antiresearch sentiments
of the 1960s was the allegation endured by Fred Sibley that his efforts
to investigate the nesting biology of condors had caused the wild pop-
ulation to cease reproducing. This attack was crystallized in an article
by Ian McMillan (1970):
Although serious breakdowns have occurred in the administration of the
Sespe Sanctuary, the closed area has functioned with dramatic effect as an
indispensable wilderness home for the condors. In the years of intensive
research which led to establishment of the refuge, Carl Koford, who carried
out the study, found a maximum of four active nests in one year. In 1967,
a total of six active condor nests were found in a new research project by
the U. S. Fish and Wildlife Service. Five of these were in or near the Sespe
Sanctuary.
This could only indicate that after twenty years in operation the refuge
was functioning most effectively in accord with its purpose. It is my con-
sidered opinion that without the special protection given this vital nesting
retreat, the California Condor would now be extinct.
It might seem from this, that a favorable and optimistic account of the
condor program can be given. Instead, an -alarming and perhaps disastrous
development must be reported. The new condor research, which began in
1966, is part of the much publicized Federal Endangered Species Program.
Its main operation, as confirmed in the discovery of six active nests in 1967,
has obviously been to find and examine condor nests. Another early result
of the project was the delivery in the spring of 1967 of a strong, healthy
young condor to a zoo in Los Angeles. This brings into focus an orientation
toward artificial propagation that has quickly become the main aspect of
the federal project (p. 95).
With the annual search for active condor nests continuing unabated,
opponents of this practice have hoped that the damage done to the condor
population might be less than the previous [Koford's] research would in-
dicate. But instead, the appeals and protests now appear to have greatly
understated the potentialities of the new disturbance. Only a single occupied
nest has been found in the two years following 1967 when the six active
nests were examined. Since that year, no nestings have been known to occur
in the Sespe Condor Sanctuary or nearby areas. The single nest that has
been found to be occupied in 1968 and 1969 is remote from the Sespe
Sanctuary by a distance of some 90 airline miles. Yet, even as it became
obvious that the research operations might be causing a general nesting
failure, this single site has been repeatedly invaded during the nesting period
(p.96).
Several comments should be offered on McMillan's assertions. First,

it is highly unlikely that Koford found more than a small fraction of
the nests active in the Sespe Sanctuary during his study. Second, as
detailed in Snyder (1983), there were indeed six condor nests docu-
mented in 1967, but contrary to McMillan, there was a total of another
six nests found active in 1968 and 1969 (with considerably reduced
field effort in 1969). Furthermore, two of the latter nests were found in
the Sespe Sanctuary. Considering the vagaries and difficulties in finding
active condor nests, these data cannot be used as evidence for a dramatic
decline in nesting activity, and even if there was a decline (as we
suspect there probably was, as part of the overall decline of the species)
it surely does not follow without further substantiation that it was
caused by research activities. In fact, an examination of Sibley'S field
notes quickly reveals that the majority of active nests discovered during
these years were not even approached until after young had fledged
from nests or after nests had failed (Sibley was under strong restrictions
not to approach nests in the early stages of breeding). Adult birds were
not even in attendance at the times of nest examination in most cases.
How nest examinations in these cases could have caused cessation of
breeding is beyond comprehension. And of the five nests Sibley entered
while they were active, only one failed subsequently, with no evidence
that failure had anything to do with the fact that the nest had been
entered. Especially interesting is the fact that while Sibley entered the
successive active nests of a pair in San Luis Obispo County once each
year from 1967 through 1969, chicks fledged each year from this ter-
ritory and the pair returned each year to nest again. McMillan's asser-
tion that Sibley's activities stopped reproduction of the species has no

basis in any data we have been able to discover.
Surely, if the brief nest entries made by Sibley had caused cessation
of breeding, we should have observed similar effects in the pairs from
which we repeatedly took eggs and young from 1982 through 1986. Yet
everyone of these pairs continued to breed year after year (most in fact
were multiple clutched each year) without any signs that our taking of
progeny, which involved considerable disturbance from numerous peo-
ple in the area and helicopter operations, gave them any second thoughts
about breeding again. In most cases courtship behavior resumed within
a couple days of an egg removal. True, the pairs moved from one nest
site to another in successive breeding attempts, but this occurred whether
or not we entered nests when they were active. Such movements were
no doubt also occurring in Sibley'S time, and in many cases he may
well have missed nestings of pairs because of this (he did not search
for nests by following adults). During our years of study, the only factor
that ever stopped any of the breeding pairs from egg laying was mortality
of one or both adults. We know of no evidence whatsoever that nest
entries can stop reproduction of the condor.
Ian McMillan also vigorously contested the validity of the October
Survey, which yielded counts higher for the late 1960s than his pop-
ulation estimate of 40 birds (Miller et al., 1965) for the early 1960s.
When the 1966 count totaled 51 individuals, McMillan wrote a strongly
critical letter to the CDFG and, in response the organizers of the survey,
invited him to attend the analysis sessions of the counts in 1967 and
1968. Some indication of the highly charged atmosphere of these inter-
pretation sessions can be glimpsed from Fred Sibley'S notes on the 1967
session:
Ian McMillan, Dr. Carl Koford, Dr. Ken Stager, Dr. Peter Ames, and Clint
Lostetter attended the Friday critique in addition to the survey evaluation
subcommittee. After about an hour presentation of methods and results Ian
asked a few questions and made a few statements but could never really
get started. At one point he stated that 21 birds seemed an unusually high
number for a single stat~on. Koford who had spent both days there said he
felt that was a very reasonable estimate. Ian then attacked the total of 12
birds during a one hour period on the same station. John Borneman pointed
out that Ben Glading and Roland Clement had had 13 condors in view at
one time during this period (the two official observers were snowed under
by photographers and visiting dignitaries and were unable to keep up with
the flow of birds. They recorded only 7 birds at one time). At another point
Ian stated that observers were probably misidentifying adult and juvenile
birds due to poor training and lack of experience. To prove his point he
cited three juveniles seen in one group at station 50B but not seen at station
50A less than a mile away. Ken Stager had identified the three birds and
both he and Carl Koford, station 50A, confirmed that there were many times
during the day when birds could be seenen from one station and not from the
other although the two sets of observers could see each other.
The consensus was that the final total [46 birds] is a conservative es-
timate from the data and an even more conservative estimate of the total
population. Koford in particular felt that birds were missed by observers
and that the limited data submitted by the observers caused us to lump
many sightings which were really of different birds. Most agreed that the
greater the concentration of birds the greater the gap would be between the
estimated number and the actual number. Finally, as in other years there
were at least four birds seen by unofficial observers or on the periphery of
the range the next day which were not included in our figure of 46. Koford
even jokingly remarked that we had almost convinced him there were 100
birds.
In spite of the high degree of consensus among participants that

the October Survey counts of the late 1960s indicated a minimum pop-
ulation of over 50 birds (official counts were 38,51,46,52, and 53 birds
for 1965 through 1969), McMillan continued to claim that the survey
was greatly overestimating the population and that the estimate of Miller
et 01. (1965) was still valid (McMillan, 1970, 1971).
Besides giving substantial evidence for a minimum wild popula-
tion size over 50 birds in the late 1960s, the October Survey also raised
concerns about the percentage of immatures in the population. Whereas
the percent of ageable condors that were immature in the 1965, 1966,
and 1967 counts were 29, 30, and 21, respectively; by 1968, 1969, and
1970, the percentage of immatures had dropped to 11, 13, and 9; and
the percentage stayed at this low level through 1974 (12, 12,6, and 12),
after which it again rose to at least 20% (Verner, 1978).
Was this apparent drop in percentage of immatures a real effect or
perhaps a sampling or observation error? If a real effect, what was the
cause? An independent estimate of percentage immatures for these
years can be derived from figures of Wilbur (1978, 1980). For the same
period (1968-1974), Wilbur reported composite probable totals of im-
matures of 10, 10, 13, 8, 8, 6, and 4 birds, respectively, while his
estimated total population declined from about 55 individuals to 40
individuals (by interpolation, based on a uniform rate of decline). These
figures yield estimated immature percentages of 18,19,26,17,18,14,
and 10 for 1968-1974, figures that average considerably higher than
those from the October Survey. The considerable discrepancy between
the two sets of figures suggests the possibility of sampling and obser-
vation errors in determinations, perhaps in both sets of values. We have
earlier argued that Wilbur's (1978) composite probable totals of im-

matures could easily be underestimates of true numbers of immatures
(Snyder, 1983), and the same could be true of the October Survey for
a variety of reasons. For one thing, distinguishing between subadults
and adults is often extremely difficult under field conditions, leading
to a large potential for error. Confusing two or three subadults with
adults in anyone year could have greatly changed the apparent age
ratios. In addition, it is important to emphasize that the percentage of
overall condor sightings that included immatures throughout the year
showed no obvious drop during the late 1960s and early 1970s (Wilbur,
1980). In our view, the assertion that that there was a true depression
in ratios of immatures to adults in the late 1960s and early 1970s rests
on an uncertain foundation.
The leap from such an assertion to a conclusion that the population
had largely stopped breeding is even more unwarranted, as changes in
ratios of immatures to adults, if valid, can result as well from changes
in rates of nesting success or from age-specific variations in mortality.
Especially heavy mortality of juveniles in one year would be reflected
in depressed immature/adult ratios for a number of years, as birds do
not reach adult plumage for 6 years. With small populations, especially
heavy mortality of juveniles could be nothing more than a chance effect.
Another possibility deserving serious consideration is that the apparent
drop in immature/adult ratios from 1968 through 1974 was a real effect
reflecting increased nesting failure at the height of the DDT era. As
documented by Kiff et 01. (1979) and Snyder et 01. (unpublished data),
eggshell thickness was uniformly depressed during the mid-late 1960s
and could have caused increased egg breakage. Although this possibility
cannot be conclusively documented from observed egg breakage and
nest success information, sample sizes of nests available for analysis
are small and the question remains open.
Regardless of cause, the apparent drop in percent immatures on
the October Surveys did fuel accusations against Sibley that his nesting
studies were causing condors to stop breeding, and had an apparently
strong inhibitory effect on nesting studies through the 1970s.
One other development of the 1960s that deserves mention was a
proposal by Carl Koford to conduct research on effects of toxic mate-
rials, such as 1080, using the Turkey Vulture as a surrogate species for
the condor. This proposal was submitted to the USFWS in 1967 and
later to the NAS· but failed to attract support. The rebuff given Koford
on this proposal can only have encouraged suspicions in some quarters
that the USFWS and NAS were not anxious to determine whether 1080
and other toxic materials were in fact major threats to condors.
3.3. The 1970s: Transition to an Intensive Approach

The early 1970s were a period of development of formal conser-
vation documents. The CDFG prepared an "Operational Management
Plan for the California Condor" (Mallette, 1970), which was followed
in 1971 by a Forest Service "Habitat Management Plan for the California
Condor" (Carrier, 1971). Then in 1974, a Recovery Plan for the Cali-
fornia Condor was put forth by the Recovery Team under the leadership
of Sanford Wilbur (U. S. Fish and Wildlife Service, 1975). The Recovery
Team itself was an outgrowth of the old Condor Advisory Committee
that was first established after Koford's study to provide recommen-
dations to the Forest Service on condor matters, but evolved into an
advisory body to the USFWS after passage of the federal Endangered
Species Acts. The California Condor Recovery Plan was the first such
plan developed for any endangered species. All the documents produced
during the early 1970s were in essence elaborations of conservation
recommendations developed in earlier decades, and for the most part
they advanced traditional noninterventionist approaches to condor
conservation.
It was not until the mid-1970s that the inadequacy of existing
approaches to condor conservation became apparent to most observers.
By this time, the worsening status of the species was becoming clear
from declining totals of the October Survey, while the failure of the
Sespe Sanctuary feeding program to increase reproduction was also
becoming evident. Causes of the decline were still in dispute, and it
was becoming obvious that not many years remained before the species
would become extinct.
With the growing appreciation that traditional approaches to con-
dor conservation were not reversing the decline, the Recovery Team
put forth in 1976 a Contingency Plan that emphasized a crucial need
for captive breeding to ensure survival of the species. This plan was
followed by a gloomy analysis of the status of the recovery effort by
Jared Verner (1978) that forecast extinction unless more active ap-
proaches were taken in conservation. Despite the existence of these
documents and the consensus they represented for members of the
Recovery Team and biologists close to the program, there was insuffi-
cient political force as yet to change the actual research and conser-
vation program. Such force only developed with the appointing of a
joint panel of nine scientists outside the program by the American
Ornithologists Union and the NAS in late 1977, a step urged by Sanford
Wilbur. This panel, chaired by Robert Ricklefs, met to review all rel-
evant data on the biology and conservation of the species and issued
a report in 1978 urging a much more intensive program, including an

emphasis on such approaches as captive breeding and radiotelemetry
(Ricklefs, 1978). This report was accepted by the USFWS; the NAS,
armed with the findings of the panel, successfully lobbied Congress to
fund a greatly expanded effort to conserve the species in late 1979.
3.4. The Modern Conservation Program

The modern program, initiated in 1980, did not represent a con-
sensus of all interested parties. In particular, there was still strong
opposition from the McMillan brothers, Carl Koford (who died in late
1979), and their followers in the Friends of the Earth (FOE), the Sierra
Club, and several local chapters of the Audubon Society. These indi-
viduals and groups united in an effort to oppose all intensive activities
with condors, and instead urged the establishment of a Sespe-Frazier
Wilderness Area and stoppage of shooting and 1080 poisoning through-
out the range of the species as adequate approaches to its conservation.
They were especially opposed to captive breeding and radiotelemetry,
repeating the traditional arguments that these approaches were too risky
and would not work, although it appeared that more than anything else
they were concerned about the degradation of the condor as a wilder-
ness symbol if man were allowed to interact with the species too closely.
Rather than captive breeding, some members of these groups advocated
"death with dignity" for the condor, should it develop that the species
could not be saved in the wild. "Captive or Forever Free" was the
provocative subtitle to a condor book that FOE published in opposition
to the program (Phillips and Nash, 1981).
In addition, there was a lack of consensus between the CFGC and
the USFWS, the two agencies with permitting authority over the pro-
gram. The degree of opposition to captive breeding was still strong
enough that the first permit for the new program issued by the Com-
mission in 1980 specified the taking of only a mate for Topatopa (some-
thing that did not actually occur until 1985). However, the first state
and federal permits did allow for the fitting of 10 condors with radio-
transmitters. But before radiotelemetry could be initiated, intensive
research on condors was brought to an extended halt by an incident
which seemed to confirm forever the "untouchability" of the species-
the death of a half-grown chick as it was being weighed and measured
to establish baseline growth curves in June 1980.
The political ramifications of the loss of this bird were so far-
reaching that they threatened in themselves to emasculate the program
indefinitely. In large measure, we personally bear the responsibility for
the loss of this bird, and it was indeed a tragic loss, both biologically
and politically. Sadly, although the loss was completely unexpected,
it was a preventable loss had better precautions been taken. The fact
that handling of late-stage condor chicks (both Andean and California
Condor) involves considerable risks of overstressing individuals-risks
that do not exist with many other species or other-aged condors-was
not known at the time, although it has become clear since then.
With the death of this chick, state permits for all intensive research
and conservation activities were withdrawn, and no such activities took
place for over two years, during which time the condor was still losing
ground and the chances of recovery were steadily dwindling. Under-
standably, with the public furor over the 1980 handling accident, the
agencies involved were forced into a defensive posture of extended
inaction. Committees were formed atop committees to review the re-
search program (there were five of them simultaneously active), but
once their deliberations were through, the inescapable conclusion was
still that the species would be lost unless intensive activities were
implemented.
During the next 2 years, research activities were limited largely to
distant observations of nesting pairs and testing of various intensive
procedures with surrogate species. Still, it is unlikely that an intensive
program would ever have resumed but for several developments in
1982. These developments were the rescue of a chick whose feeding
rates were dropping strongly when one parent disappeared; the devel-
opment of photocensusing estimates of the population size; and the
conclusively documented capacity for replacement clutching in wild
pairs. The successful bringing of a chick into captivity demonstrated
that the sensitivity of the species did after all have limits, while the
photocensusing efforts demonstrated that the species was much worse
off than many had assumed. Finally, documented replacement clutch-
ing opened the doors to starting of a captive population with minimal
impact on the wild population by taking eggs. Furthermore, in late 1982
the first two free-flying condors were trapped and fitted with radio-
transmitters without any detectable negative effects on their behavior.
One of the two was a breeding male adult, who, despite the oft-repeated
fears of opponents that radios might cause pair breakups, proceeded to
breed on schedule with his mate the following year. Without question,
1982 was a most crucial year in conservation of the condor, and in the
following years considerable progress was made in establishing a cap-
tive population and gaining information on causes of decline of the
wild population.
While the heartening progress of 1982 and 1983 allowed renewed
optimism about preservation of the species and a temporary subsidence

in the fever pitch of conflict over conduct of the program, controversy
again broke out in the summer of 1983-this time within the research
program. The issue was whether the chick produced from a third egg
laid by the Sespe Sanctuary pair should be allowed to fledge naturally
in the wild. The director of the CDFG was on record as favoring at least
one natural fledging in the wild each year. The NAS favored radioing
the chick to learn more about the behavior of fledglings, while we and
others argued that the bird should be taken captive.
The reasons for our position were severalfold. First, from what we
had learned about replacement clutching and annual nesting of the
species, there was virtually no chance with natural fledging of the chick
(unless it died) that its parents would breed the following year. The
chick had hatched only in early July and would surely be dependent
on its parents through the following spring. By allowing the chick to
fledge naturally, we would in effect be consciously preventing the lay-
ing of two, possibly three, eggs the next year by the pair. Since the pair
was not yet well represented by progeny in captivity and could at any
time be lost through mortality, and since we were only in the initial
stages of establishing a viable captive population, this seemed a stiff
price to pay for a wild fledgling.
Additionally, with the loss of a late-stage chick during handling
in 1980 still fresh in mind, we were strongly opposed to the handling
of another late-stage chick for the length of time it would take to fit it
with radios. We had not yet succeeded in radioing any condor, Andean
or California, in less time than it took for the 1980 chick to expire, and
this was radioing relatively easy-to-handle older birds, not struggling
chicks. If another chick were to die from stress of handling, this would
probably be the end of the program (and very likely the species with
it). Veterinarians at the San Diego and Los Angeles Zoos uniformly
opposed the taking of such a risk (they had just had an Andean Condor
chick collapse on them without warning and with only brief handling).
Members of the CFGC were also opposed. Thus, the radioing of a chick
had no political viability, as it would have to be approved by this body.
In spite of these considerations, the USFWS decided to side with
the NAS and proposed radioing the chick and allowing it to fledge
naturally, claiming that the conservation program had become seriously
"unbalanced" with too much emphasis on captive breeding and not
enough on radiotelemetry. The USFWS indicated confidence that it
could radio a chick safely and that the important research advances
that could be made with a radioed chick fully justified any risks in-
volved, including the loss of reproduction by the pair the next year.
CONDOR llIOLOC;Y AND CONSERVATION 237
After months of negotiation too complicated to repeat here, the

USFWS finally agreed with the CFGC that the bird should be taken
captive, and it was. As predicted, the parent birds did breed again the
following year, producing two more offspring (both taken captive as
eggs), but this proved to be their last breeding, as the male adult per-
ished over the winter of 1984-1985. If the 1983 chick had been allowed
to fledge in the wild and had survived, there presumably would now
be only two progeny of this pair in captivity (possibly three if the 1983
fledgling had subsequently been trapped into captivity), and the captive
flock would now presumably include three (two) fewer individuals.
By late 1983 and 1984, the encouraging success with multiple
clutching of the wild pairs and the continuing survival of these pairs
led to sincere hopes that it might soon be reasonable to begin releases
of some captive-raised birds into the wild in an effort to bolster and
sustain the remnant wild population. Meanwhile, it was still reasonable
to believe that continuing efforts to elucidate the as-yet largely un-
known causes of decline of the wild population might ultimately allow
enough reduction in the factors stressing the population to permit its
recovery. The Recovery Team developed an early release plan, which
was later approved by the USFWS and the CFGC, in which releases of
captives from any family line might begin as soon as five progeny from
that line were achieved as permanent captives. Captives would be re-
leased to the wild using techniques developed by Mike Wallace with
Turkey and Black Vultures (Coragyps atratus) in Florida and Andean
Condors in Peru (Wallace and Temple, 1983, 1987).
By the end of 1984, two family lines were represented by five
progeny apiece in the captive flock. Thus, it appeared that releases of
some young from these family lines might be feasible in 1985 if both
pairs could be multiple clutched in that year.
Unfortunately, the winter of 1984-1985 proved catastrophic for
condor survival in the wild, and neither of the pairs with five progeny
apiece in captivity endured to the breeding season of 1985 (both lost
male adults). Furthermore, two other pairs active in 1984 were also lost
(one lost the female adult, and the other lost both adults). In addition,
a new pair that formed in early 1985 also lost one member before egg
laying and, altogether, there was only a single breeding pair left in the
population by the middle of the 1985 breeding season. A full 40% of
the population had perished in the space of a few months, and the
reproductive potential of the population was nearly destroyed in the
process.
Plans for early release of captive progeny, based on continued mul-
tiple clutching of wild pairs, suddenly became irrelevant in the minds
of many observers, and a year-long political battle over the fate of the
last wild birds began. In retrospect, this was the most extraordinary
chapter in the entire history of condor conservation. We recount the
major events of this turbulent period in some detail, as there were many
aspects to the battles that have been seriously misunderstood.
3.4.1. The Crisis of 1985-1986

First indications of the catastrophic mortality of the winter of
1984-1985 came when we initiated watches of the nesting territories
in January 1985. It became immediately apparent that most of the ter-
ritories were now occupied by only single birds. We immediately ex-
panded our photocensusing efforts greatly, but none of the missing birds
turned up anywhere in the range of the species during the weeks that
followed. By March, we were convinced they had perished, and we
sounded the alarm that six birds from the population had apparently
been lost and that mortality had unfortunately hit the breeding pairs
especially hard. It was clear that on the basis of the approved plans of
the Recovery Team, the minimum requirements for an early release
program could not be met and, together with other participants in the
program, we suggested that the situation was now so serious that it
seemed essential that the remaining wild birds should be taken captive.
The wild population was clearly an inviable entity while the captive
population was still much too small and too low in genetic diversity
to be considered adequate-far below the level of adequacy that had
been defined by the Recovery Team in 1984. Everything now seemed
to depend on establishing a viable captive population, as there was no
way one could hope to overwhelm the sort of mortality just seen in the
wild population with an early release program.
The responses to our suggestions varied from disbelief and angry
antagonism to acceptance. Some observers, including administrators in
the USFWS and NAS, informed us that it was much too soon to con-
clude that the birds apparently missing were truly missing and that we
would have to wait until late summer to be sure. In their view, the
birds might have just moved somewhere else, abandoning their mates
and territories (we knew this to be most improbable). Others, who were
more accepting of the census information, were convinced that bringing
in the last wild birds was politically impossible and that it would doom
habitat preservation efforts, even though the USFS pledged publicly at
this time to maintain the sanctuaries so long as there were reasonable
chances for reintroduction efforts there. We had difficulty understand-
ing how habitat preservation efforts might take precedence over the
critical need for establishing a viable captive population without which

habitat for the species would be irrelevant, but the argument that the
last birds had to be left in the wild to save habitat attracted many
supporters initially. In addition, NAS researchers and supporters ar-
gued that birds had to be left in the wild to preserve the foraging and
nesting traditions of the wild population. Whether or not some or all
of these traditions were worth saving, we doubted they could be better
preserved by leaving birds in the wild than by taking them into "pro-
tective custody," with options for later return to the wild left open.
In April 1985 the Recovery Team met to consider the crisis and
decided to ask a broad sampling of the nation's most experienced pop-
ulation geneticists to evaluate the genetic adequacy of the existing cap-
tive flock. The unanimous conclusion of these consultants was that
because of the limited number of family lines represented in captivity,
the existing flock could not be considered to possess a sufficiently safe
level of genetic diversity to guarantee long-term survival of the species.
In addition, every geneticist consulted by the Recovery Team urged in
writing that even to approach a genetically adequate situation, all the
remaining wild birds should be added to the captive flock. This rec-
ommendation gained even greater force from the likelihood that some
of the captives might never become breeders.
Shortly after these recommendations were received, preliminary
results on the extent of blood enzyme polymorphism in most of the
remaining condors were obtained from Kendall Corbin (personal com-
munication). Results indicated very low heterozygosity in comparison
with levels found in other bird species, suggesting that the remnant
population was already seriously deficient in genetic diversity.
Acting on the recommendations of the geneticists and on the evi-
dence for catastrophic losses over the winter of 1984-1985 (no one was
still arguing that the missing birds might be alive), the CFGC authorized
the trapping of all the last wild condors in early June 1985 and requested
the USFWS to consider similar action. The USFWS followed with ini-
tial approval to bring in three of the nine remaining wild birds, and
these were taken captive during the summer of 1985.
Disposition of the other six wild condors was debated vigorously
through the summer and fall of 1985, with the USFWS initially ad-
vocating leaving all birds in the wild, while the CFGC continued to
press for their immediate capture. In addition, the USFWS reversed at
this time its earlier backing of the Recovery Team position that releases
to the wild should not involve captives having fewer than five siblings
in captivity, and now proposed, with support from the NAS, but not
from the CFGC, that three captives should be released to the wild in
the near term. The USFWS-NAS position at this time was based on an
assumption that mortality risks for birds in the wild could be greatly
reduced by an intensive feeding program with clean carcasses that was
initiated on Hudson Ranch in the spring of 1985 (despite strong evi-
dence from the earlier feeding program of Wilbur that one could not
reasonably get the wild population to abandon well-established feeding
traditions, as long as food continued to be available in many other parts
of the foraging range).
However, by the time the USFWS-NAS proposal to go ahead with
releases of captives was announced, the five birds that had been held
at the Los Angeles Zoo for potential release had already been taken out
of prerelease isolation. In accordance with planning documents adopted
only a few months earlier by the Recovery Team, the USFWS, the CFGC,
and the NAS, these birds clearly did not meet the criteria for release
and were to be used instead for captive breeding. Following the unan-
imous reaffirmation of this policy at the Recovery Team meeting of
April 1985, there was no reason to continue prerelease conditioning.
The birds were taken out of isolation and now exposed to normal cap-
tive-breeding conditions under which they did see keepers and were
allowed to associate them with food (a situation to be avoided in birds
destined for release).
When the USFWS-NAS proposal to go ahead with releases anyway
materialized several weeks later, it came as a total surprise to nearly
everyone involved with the program in California (including ourselves).
Furthermore, neither the USFWS nor the NAS admitted that they were
now turning their backs on plans they had just agreed to. Instead, they
publicly accused the Los Angeles Zoo of having unilaterally sabotaged
the release program by taking prerelease birds out of isolation, an al-
legation that continues to be circulated to this day.
While the Recovery Team was unanimous at its April 1985 meeting
that there should be no near-term releases of captives to the wild, it
was split on the issue of how many birds should be brought into cap-
tivity. However, at the August meeting of the Recovery Team there was
a consensus that at least three of the controversial six birds should be
taken. By the end of the year an informal poll of team members indicated
unanimity in favoring the capture of all remaining wild birds, but the
USFWS central command prohibited further meetings of the Recovery
Team after August, as it pursued its own convictions as to the best
conservation strategies for the species.
The AGU Condor Committee, which met to consider the crisis in
May 1985, took a stance similar to the initial position of the Recovery
Team by recommending no near-term releases of captives to the wild
and by failing to take a clearcut stance on disposition of the last wild

birds. This committee stated that they felt all the wild birds should be
taken captive on biological grounds, but that to preserve the existence
of the research program and to aid in habitat preservation efforts, several
birds should be left in the wild, regardless of their poor chances for
survival.
One of the more unfortunate aspects of leaving any birds in the
wild was the fact that most of the remaining wild birds were male,
while the captive flock had an excess of females. Thus, each male left
in the wild deprived the captive flock of a potential pair, and as was
recognized by the AOU committee, the demographic potentials of the
captive flock were as important as, if not more important than, the
genetic potentials. The number of potential heterosexual pairs in cap-
tivity by late summer of 1985 was eight. Bringing in the last remaining
birds would have added 50% to this potential in the near term, a far
from negligible increase, both genetically and demographically.
In late August, a compromise was reached between the USFWS
and CFGC entailing the capture of three more wild birds for captive
breeding and an agreement by both agencies to pursue an "aggressive
policy" of releases of captives to the wild. Exactly what an "aggressive
policy" of releases implied was not clarified. An important component
of the compromise was an agreement that all wild condors would be
brought into captivity if one more wild bird perished.
Nevertheless, although the USFWS had agreed to fully authorize
the trapping of three more birds by mid-September, it did not do so,
primarily because of NAS opposition (including the threat of a lawsuit)
to the August compromise. Authorization by the USFWS for the capture
of three additional wild condors did not occur until late October, when
to break the impasse, the CFGC specifically agreed to consider release
of three condors to the wild in the spring of 1986, if three birds suitable
for release were available at that time, and if agreement could be reached
as to where the release might take place. In its October statement to
the CFGC, the USFWS failed to reaffirm its earlier support for taking
the rest of the wild population captive in the event of any more mortality
of wild condors, although this option was left open in the Environ-
mental Assessment written to cover the situation.
In early November 1985, strategies for the California Condor were
discussed at length at the Third International Vulture Symposium held
in conjunction with the Raptor Research Foundation meetings in Sac-
ramento. As a result of these discussions, a resolution was adopted on
a nearly unanimous basis by the meeting participants that all the re-
maining wild condors should be taken captive as soon as possible; that
no releases of captives should be attempted until a healthy, self-sus-

taining captive population was achieved; and that releases of California
Condors to the wild, once they became advisable, should be limited to
regions that offered effective protection from detrimental human influ-
ences. Although this resolution represented a strong consensus of a
large fraction of the biologists directly involved in raptor and vulture
conservation worldwide, there was no immediate comment from the
USFWS or NAS.
In late November the female of the last remaining wild breeding
pair, a bird not yet authorized for the captive breeding program, was
captured to replace her defective radiotransmitters. A blood sample
taken at this time, but not analyzed until after the bird was released,
proved to be heavily contaminated with lead. This finding led the vet-
erinarians and toxicologists advising the program to recommend that
the bird be recaptured for treatment. The detection of high lead levels
in this condor (she had had low lead levels when captured earlier in
the fall) proved to be a crucial development in convincing the USFWS
that the remaining wild condors were still at high risk, especially since
this particular bird was one that the NAS and some individuals in the
USFWS had claimed was at very low risk from such poisoning because
of her supposedly "safe" foraging habits and range.
In mid-December 1985, Richard Smith, Associate Director of the
USFWS, sought and obtained a reversal of USFWS policy. The USFWS
announced it now concurred with the longstanding position of the
CFGC that all the remaining wild condors should be brought into cap-
tivity and that there should be no near-term releases of captives to the
wild. The reversal was attributed primarily to the high lead levels in
the November-trapped condor but also to the fact that there were no
captive birds behaviorally suitable for release in 1986, and to the fact
that a new pair bond was forming in the wild between one of the birds
slated for capture and one of the birds to be left in the wild. However,
before trapping could begin, the NAS filed suit to obtain an injunction
against capture of the last wild birds, alleging that the USFWS's de-
cision was arbitrary and capricious, and that taking the last birds captive
would doom habitat preservation efforts. The NAS won the first round
in the courts, but was ultimately defeated on appeal.
In the meantime, the lead-poisoned bird that was the primary cause
of the USFWS policy reversal was finally recaptured on an emergency
basis and brought into intensive care at the San Diego Zoo. It was too
late. Despite round-the-clock efforts by the staff of the zoo to detoxify
and bolster the now-emaciated bird, she died on January 18. With legal
restrictions on trapping removed, efforts to capture the remaining five
CONDOR BIOLOGY AND CONSERVATION
wild condors began in the summer of 1986, and all had been captured
by the spring of 1987.
3.4.2. Acquisition of the Hudson Ranch

Closely tied in with the efforts of the NAS to prevent trapping of
the last wild condors was the effort of this organization to persuade
the federal government to purchase Hudson Ranch, a 50-km 2 area of
grassland in the southwestern San Joaquin Valley foothills, as a crucial
refuge for condors. This effort was first launched in late 1982, when it
became apparent that Hudson Ranch was receiving considerable use
from condors and plans were announced by its owners for development
of the ranch into a residential-agricultural complex. At that point, the
principal problems of the condor were still almost completely specu-
lative, and there was no reason to consider Hudson Ranch as anything
other than an important and positive component of the foraging range.
We fully supported the original NAS initiative on purchase of this
ranch, although we would later come to see Hudson Ranch more as a
cause of than the solution to the condor's difficulties.
Once the campaign was started to acquire the ranch, there was no
turning back, and the image of the ranch ultimately became unrecog-
nizable as more and more arguments of less and less merit were used
to justify the purchase. In the view of its supporters the ranch became
not just a heavily used foraging area, but an ideal and finally "the only"
place that it made any sense to release condors to the wild (Anonymous,
1985), in spite of the fact that the ranch is nearly 30 km from the nearest
known condor nest site and is surrounded by other ranches on which
a variety of activities dangerous to condors are practiced. In time, as
we gained specific knowledge of the threats faced by the species, we
came to realize that Hudson Ranch was in fact one of the very worst
places to release captives, but by then, so many people and organiza-
tions had gone on record praising the virtues of the ranch there was no
graceful retreat left. The ranch was ultimately acquired as the Bitter
Creek National Wildlife Refuge. Unfortunately, unless many hard-to-
achieve changes occur in the management of surrounding ranchlands,
it is doubtful that Hudson Ranch will ever fulfill the hopes of its sup-
porters of becoming an important and positive part of condor habitat
of the future.
Elements of the campaign to acquire Hudson Ranch may remind
the reader of the efforts to acquire the Sespe Sanctuary. The biology of
the species became subverted to the goal of habitat acquisition and
dogma replaced good data as supporters proclaimed the critical nature
of the acquisition to survival of the species. Perhaps this is the only

way sanctuaries can ever be acquired, but in the case of Hudson Ranch,
the disparity between reality and propaganda became especially great.
In the efforts to justify the ranch, it became the ultimate location
for subsidizing the wild population with clean food, thus effectively
countering lead poisoning and other associated threats (note here that
we are no longer talking about a natural unmanaged condor population
as advocated by Koford and Miller et a1. and their followers). At times
during the height of the 1985 controversies, claims were made that
condors were getting most of their food from Hudson (something that
Wilbur was never able to come close to in his feeding program next to
the Sespe Sanctuary), although no plausible analyses were presented
to substantiate such claims (Anonymous, 1985).
Since, however, there was a considerable amount of data available
on how much food captive condors need to eat to maintain body weight,
on their crop storage capacities, and on how long it takes a wild condor
at a carcass to fill its crop, it appeared that data adequate to analyze
what fraction of wild condor diet was being supplied by carcasses on
Hudson must exist in the detailed records of the CRC carcass observers.
Data from July 1985 were far more detailed and comprehensive than
for other months and July is normally a peak month for condor activity
on Hudson, so we anlayzed these data for food consumption taking
care to err on the high side when there was any question about how
much a particular condor had consumed at the baits. Results were not
encouraging. A generous interpretation of the overall records indicated
that the wild population was getting only about 20% of its food needs
from the provided carcasses; if this fraction could be converted into
the amount of mortality reduction one might expect from the feeding
program, it was completely inadequate to protect the wild population
from more than a small fraction of the threats faced on the foraging
range. Although we circulated this analysis on an informal basis in
September 1985, faith in the feeding program remained high until late
1985 when lead poisoning of a bird known to feed heavily on Hudson
ended all arguments.
4. THE ROAD AHEAD
4.1. Prospects for Success in Captive Breeding

The future of the California Condor now rests entirely in the realm
of captive breeding, but as of this writing only one chick has ever been
produced by captive parents, a bird hatched in early 1988. In large part

this is not surprising, as up until the last three years, adult males had
never been caged together with adult females, and the present captive
flock consists mainly of immatures. Nevertheless most observers believe
the species will breed readily in captivity, judging from the captive-
breeding success that has been obtained with other cathartids, espe-
cially Andean Condors (see references cited in Verner, 1978, and Sny-
der, 1986).
Captive reproduction of Andean Condors has been the subject of
intensive research at the Patuxent Wildlife Research Center since 1966
(Carpenter, 1982), and the species has now been bred in numerous
zoological institutions. At Patuxent, it has been possible to obtain two
eggs per pair annually on the average, and some institutions have had
pairs lay as many as three or even four eggs in a year. Thus, it appears
likely that replacement clutching and annual nesting are reasonable
expectations for captive as well as wild California Condors.
Nevertheless, we believe it is possible to be overoptimistic about
captive reproduction of California Condors. The last pairs in the rem-
nant wild population exhibited high rates of reproductive abnormalities
and, since the birds in the captive flock are largely progeny of these
birds, or in some cases are the very birds themselves, it is reasonable
to expect problems with reproductive abnormalities in captivity as well.
Great success in captive breeding of surrogates does not always translate
into great success in breeding endangered species, and the causes for
this, while rarely identified with certainty, may commonly be the rel-
atively poor genetic quality of the individuals which have been avail-
able to establish captive flocks of endangered species. Thus, while Pa-
tuxent personnel have been able to breed nonendangered races of Sandhill
Cranes (Grus canadensis) with facility, they have had much more dif-
ficulty with the endangered Mississippi Sandhill Crane (G. c. pulla)
and the endangered Whooping Crane (G. americana) (Scott Derrickson,
personal communication). Similarly, while Hispaniolan Parrots (Ama-
zona ventralis) have bred freely in captivity, captive breeding of the
endangered Puerto Rican Parrot (A. vittata) has been much more dif-
ficult (Snyder et aI., 1987). It is only reasonable to expect that captive
breeding of California Condors may be less successful than that of
Andean Condors.
As can be seen in Table III, the number of family lines in the present
captive flock is not large, and the species is unquestionably in a genetic
bottleneck at the present time. Whether it will pull through the bottle-
neck successfully remains to be seen. While we remain basically op-
timistic that it will, judging from the recovery of other bird species
reduced to lower numbers than the low point for the condor, it is well
to anticipate that recovery may be slower than some people envision,
and may, in the worst case, not even be possible. Had the San Diego
Zoo been allowed to continue in its efforts to begin captive breeding
of California Condors more than 30 years ago, prospects for the species
would almost surely be considerably brighter now.
One of the most frustrating aspects of many endangered species
programs has been the political difficulties in beginning captive breed-
ing efforts before species have been virtually lost. By then, the chances
of successful captive propagation have often been considerably re-
duced, both because of the reduced reproductive vigor of the last in-
dividuals and because of insufficient time left to research and develop
the specific techniques necessary for success. Few conservationists have
enough background in captive propagation of wildlife to fully under-
stand the handicaps put on the process by excessive delay, and with
species after species captive breeding has only been started when there
have been no other alternatives left. It is no surprise that many of these
final-hour attempts have been unsuccessful.
4.2. Prospects for Release of California Condors to the Wild

The fact that the mortality rate of the remnant condor population
proved to be considerably worse than was suspected even a few years
ago has raised strong doubts as to the safety of the last habitats occupied
by the population and as to whether releases of captives, once they
become advisable, should be made into these habitats. Essentially all
documented mortality of free-flying condors in recent decades has been
limited to the traditional foraging areas in the San Joaquin Valley foot-
hills and to roosting areas associated with these foraging areas, and it
has become increasingly clear that effective reductions of the mortality
threats in this region pose enormous practical difficulties. Although a
fully comprehensive identification of the mortality factors affecting the
remnant population was not achieved before the disappearance of that
population, the principal apparent threats documented in recent years
have turned out to be especially difficult to control, at least in the short
term.
Collision with powerlines, for example, appear to be a very difficult
problem to solve. Powerlines crisscross the recent range of the species
in many regions, and the expense of burying or rerouting these lines
would be prohibitive. Unless effective ways are found to reduce the
dangers represented by these lines by other means, such as making the
existing lines more visible to wildlife, perhaps by attachments, coloring,
or other methods, the only solution to this problem may be to reestablish

condor populations in areas lacking overhead wires in the first place.
Experiments are now being contemplated and started in Colorado,
Nebraska and Spain to test ways of increasing conspicuousness of
powerlines to large cranes and vultures (R. Drewien and J. Garz6n,
personal communication), but it remains to be seen how effective such
developments may prove in reducing mortality.
Effective reductions in the threats of shooting and lead poisoning
in the recent condor foraging range also appear to pose enormous dif-
ficulties in the present social environment. Not only are there powerful
special-interest groups that oppose restrictions on shooting and hunting
in this region, but the problems of enforcing any such restrictions would
be immense, considering the probability that most of the shooting and
hunting in the recent condor range is already illegal and unregulated.
Broad restrictions on hunting and shooting in the name of condor con-
servation may do little other than ensure retaliation against the very
species one wants to protect.
Unfortunately, the primary threat of lead poisoning to condors
appears to come from bullet fragments, rather than lead shot, and no
practical alternatives to lead bullets are available for hunting of deer
and other large mammals. Thus, unlike the situation with lead poison-
ing of waterfowl (which can be hunted with steel shot) the lead-poi-
soning threat to condors cannot be quickly countered by a switch to
steel ammunition. Although steel-jacketed lead bullets are used by the
military, they are not legal for civilian use and have properties making
them unsuitable for hunting of game (high crippling loss rates). More-
over, since they have lead components, they may still be a threat to
condors. Perhaps the day will arrive when copper or some other sub-
stitute material will displace lead in bullets, but unless such substitutes
offer practical or economic advantages over lead ammunition, it may
be very difficult for them to replace lead without government action
(such as proved necessary in the case of leaded gasoline). Unfortunately,
the condor is the only wildlife species known to be suffering a poisoning
threat from lead bullets, so there is no widespread lobby within the
wildlife community to pressure for the development of alternatives to
lead bullets.
The alternative of attempting to control threats of shooting and
lead poisoning by purchasing or leasing a major fraction of the recent
foraging range means an investment of many hundreds of millions of
dollars. Such monies are not presently available, nor are they likely to
become available quickly. One of the principal difficulties is that many
ranchers within the recent condor range derive a considerable fraction
of their income by leasing out hunting rights. Buying out these hunting
rights to stop threats of shooting and lead poisoning would be an in-
ordinately expensive proposition. Moreover, assuming hunting rights
were acquired, there would be additional large investments necessary
in game law enforcement on these lands. In the near term, the most
effective way to counter threats of shooting and lead poisoning, like
the threat of collisions, may be to reestablish the condor in places where
these threats do not exist in the first place.
Do any such places exist, and can condors be confined to these
places? In February 1986, we coauthored, with a number of other par-
ticipants in the condor program, a proposal that addresses the potentials
of reintroducing California Condors into two areas of California that
appear to be relatively free of all known mortality threats to the species.
This proposal has come to represent the basis 'for recent Recovery Team
and USFWS planning for the species, and we believe it represents a
very practical near-term solution to conservation of the species.
The areas we have recommended for future reintroductions of Cal-
ifornia Condors are the Sespe and Sisquoc Condor Sanctuaries and
surrounding well-protected areas. At first sight, it might seem perverse
to suggest reintroducing the species into regions from which it has just
disappeared for all the reasons discussed so far. But we believe these
represent the best places for first tries at reintroduction for a number
of important reasons. First and foremost, these regions are already well
protected from the major known mortality threats to the species, and
with minimal effort and minor political difficulties could become com-
pletely safe from these threats. Second, these areas have the highest
concentrations of suitable nest sites known anywhere in the former
range of the species and they formerly supported high concentrations
of breeding condors. Third, the density of one of the principal natural
enemies of the condor, the Golden Eagle, is very low in these areas,
primarily because they are areas covered largely by chaparral, a habitat
type unsuitable for eagles. Fourth, and perhaps most important, though
it sounds counterintuitive, there is no significant natural condor food
supply to be found in these regions or in surrounding buffer regions.
Because of the absence of a natural food supply in these regions, the
condors nesting there in past decades developed traditions to forage
elsewhere, and it is surely the use of these other areas that has resulted
in the near-extinction of the species. But if naive condors were intro-
duced into the Sespe and Sisquoc Sanctuaries and were provided with
reliable local food supplies, there is every reason to expect that they
would never find reason to leave these areas and forage in dangerous
areas elsewhere.
While introductions into these sanctuaries would imply a long-

term commitment to feeding programs, such programs are very easy
and inexpensive to run and, once birds are reestablished, are essentially
the only investment, outside of continued law enforcement, that would
have to be made in sustaining the populations. Feeding programs are
a commitment that will also be faced by releases in all other existing
potential release areas, at least initially and very likely indefinitely.
Until the day a true megasanctuary might be established with an ade-
quate natural food supply, nesting sites, and freedom from mortality
threats, there may not be any practical alternatives.
Thus, we believe that at least in the near future, the most practical
way to counter the mortality problems that have brought about the near
extinction of the condor is to avoid these problems spatially by re-
building populations and foraging traditions in limited secure areas
isolated from other potential foraging areas by substantial buffer areas
in which food supplies are sufficiently low that they would not serve
to decoy birds from the secure areas.
Movements of released vultures can only be controlled if the food
supply is under full control. This is one of the reasons why releases in
an area such as Hudson Ranch offer little promise of success. Even if
one could make Hudson Ranch itself perfectly safe from mortality threats,
it is surrounded on all sides by continuous foraging habitat with un-
controlled food supplies that can ultimately be counted on to decoy
birds away from the ranch and onto surrounding dangerous terrain.
This is especially true because of the extremely high populations
of Golden Eagles that inhabit this area year-round. Golden Eagles are
normally dominant to condors at carcasses and commonly control car-
casses to such an extent that condors are forced to range widely in
search of food. We have commonly observed condors giving up and
moving elsewhere after waiting for eagles to finish at carcasses. Unless
one were to commit oneself to massive perennial eagle-control efforts
in the Hudson Ranch region, one could confidently predict rapid ex-
pansion of the range of any condors released there. As naive young
condors have special difficulties competing with eagles, the problem
of releasing young condors to the wild in this region would be especially
severe.
By contrast, Golden Eagles are uncommon in the Sespe and Sisquoc
Sanctuary regions. Despite a condor feeding program carried on con-
tinuously on the edge of the Sespe Sanctuary from 1971 to recent years,
no buildup has been seen in Golden Eagles there, beyond the single
pair that occupies the region, probably mainly because the grassland
habitat in this region is quite limited and separated from other suitable
Golden Eagle habitat by substantial distances. The large numbers of

wandering eagles found in the San Joaquin Valley foothills do not move
across the wide stretches of chaparral to encounter the sanctuaries with
any frequency.
The practicality of confining condors to such release areas has
already been tested with a very similar species, the European Griffon
Vulture (Gyps fulvus). During the past eight years, Michel Terrasse
(Terrasse, 1985) has succeeded in establishing a growing population of
these vultures in the Massif Centrale of France, a region from which
the species was extirpated several decades ago primarily by poisoning
for predators (which is no longer carried on). The released population
has developed very short-range foraging patterns despite the normally
expansive movements of natural populations of European Griffons. There
does not appear to be any innate "wanderlust" in the released birds;
Terrasse, who has been trying to expand their range, has had great
difficulty in getting them to move away from the general release vicinity.
The release area contains abundant natural nest sites, which are being
used by the birds, but the birds are still almost completely dependent
on a provided food supply. The "natural" food supply in the region
(primarily sheep) is not reliable, especially in winter, and it appears
that this population will always have to have some special help, al-
though the management now practiced is extremely low in cost and
the population is increasing rapidly.
On recommendations of the California Condor Recovery Team, the
USFWS has recently decided to implement a temporary release program
of female Andean Condors into the Sespe and Sisquoc Sanctuaries to
test the suitability of these areas further for California Condor reintro-
duction. This idea, first proposed by Cathleen Cox of the Los Angeles
Zoo, offers the potential of direct evaluation of a number of questions
with by far the best surrogate available for the California Condor. Of
major interest is the extent to which released Andean Condors can be
induced to develop favorable limited foraging and roosting traditions.
Such releases could also be expected to reveal what practical problems
may exist in releasing California Condors in chaparral habitat, without
sacrificing any California Condors in the process. At best, it will be
several years before significant numbers of captive-reared California
Condors are available for release; meantime, surrogate releases of An-
dean Condors may significantly improve the chances of success of the
first California Condor releases. Abundant captive Andean Condors are
available for such releases from zoological institutions around the coun-
try, and the procedures for such releases have already been tested quite
extensively and successfully in Peru by Mike Wallace (Wallace and
Temple, 1987). The released Andean Condors will be returned to cap-

tivity when releases of California Condors commence.
If subsidized wild populations of California Condors can be estab-
lished in the Sespe and Sisquoc Sanctuaries, the same approach can
probably be used to establish the species in other areas, such as the
Grand Canyon of Arizona (see Rea, 1981). Aside from the aesthetic and
educational values of such free-flying populations, they represent a
considerable economic saving over a strict captive-breeding approach
in the near term. Terrasse's costs of maintaining a released population
of European Griffon Vultures in France run about $25,000 per year
(personal communication), while current maintenance of captive pop-
ulations of California Condors at the San Diego and Los Angeles Zoos
costs each institution about $200,000 annually.
4.3. Ultimate Goals of Condor Conservation

Even if the California Condor could only be saved as a permanent
resident in captivity, we believe that this would still be a worthwhile
goal. But if the species can be saved in captivity, there is little doubt
that it can also be gotten back into the wild, at least in food-subsidized
populations in secure places like the Sespe Sanctuary.
Is it realistic to hope for wild condor populations completely free
from conscious human management? Presumably such populations
would have to have adequate food supplies, nest sites, and considerable
freedom from mortality factors. Are there any places fulfilling these
requirements still in existence, or are there any places that with rea-
sonable and affordable efforts could be converted into areas fulfilling
these requirements?
In part, the search for an answer to this question depends on de-
velopments that are very hard to predict, such as the future of cattle
ranching, deer hunting, predator control operations, and potential change-
overs to non-lead ammunition for hunting of game. In part, the answer
depends on whether the public might desire to have condors dependent
on carcasses of domestic animals and hunter-killed wildlife or whether
there is adequate public support to develop condor populations func-
tioning as parts of totally natural ecosystems. The former situation has
been the real (although ultimately nonviable) situation for the species
for many decades. No one alive today can remember the latter situation.
Yet the latter situation is one that we find much more worth fighting
for. In our opinion, viable free-living condor populations dependent
on herds of domestic livestock and hunter-killed wildlife would be
very difficult to achieve under present economic and political condi-
tions, and may actually be inferior aesthetically to free-living popula-

tions dependent on deliberate feeding programs in secure sanctuary
areas. Both sorts of populations are, in the final analysis, dependent
on unnatural food supplies. The only real difference is that in the one
case the man-supplied food supply is unreliable and inherently dan-
gerous; in the other it is regulated and safe. In fact, to make the former
case work, the expense and amount of human "management" of the
situation would unquestionably be orders of magnitude greater than
what would be needed for the latter case.
Are totally natural condor populations dependent on carcasses of
natural indigenous vertebrates achievable? Some people have suggested
that totally natural populations might be feasible on some of California's
Channel Islands, which have a substantial natural food supply in the
form of carcasses of marine birds, fishes, and mammals washed ashore.
Some of these islands are also quite well protected, being in National
Park Service and Nature Conservancy ownership. Unfortunately, at the
present time, at least, the food supply represented by marine vertebrates
in this region is one of the most pollutant-contaminated food supplies
known anywhere (Gilmartin et a1., 1976; Schafer et a1., 1984; Garcelon
et a1., 1988), and we fear this could well preclude successful estab-
lishment of condors.
Elsewhere, in searching for regions with adequate and protected
natural food supplies, the choice becomes very limited. Certain Na-
tional Parks, such as Yellowstone, have large native herbivore popu-
lations, but whether they are large enough and can provide sufficient
carcasses throughout the year to sustain viable condor populations is
questionable. No condors are known from the region of Yellowstone
either historically or from the fossil record, so it is doubtful this region
would be adequate.
Grand Canyon, an often-mentioned potential release area, now has
mainly feral burros (Equus asinus) and mule deer as a potential "nat-
ural" food supply, though the burros are not indigenous to the area. It
is also quite uncertain that the region has a food supply sufficient to
support condors without supplemental foods. As Emslie (1987) pointed
out, the condors known from the Grand Canyon in the fossil record
disappeared at the end of the Pleistocene, when a great variety of large
mammals also disappeared, and whether the natural food supply in
the region was adequate after that point is questionable, although there
are a number of published condor sightings for this region from the
past century (Rea, 1981). While we are very much in favor of attempts
to reestablish condors in Grand Canyon, supplemental feeding will very
likely be necessary here.
CONDOR BlOLOCY AND CONSERVATION 253
Where else? The choice of existing protected locations with good

populations of large indigenous vertebrates ends about here. But this
is not the end of possibilities. What we would like to propose is that
a more promising approach to reestablishing condors in totally natural
ecosystems may be to recreate the ecosystems of the past in well-chosen,
well-buffered regions. These would have to be reasonably productive
ecosystems to sustain an adequate food base for the species, and pre-
sumably the impetus toward re-creation of such ecosystems might be
greatest if they might at the same time lead toward the preservation of
other endangered species such as wolves (Canis lupus) and grizzly
bears. They would have to include large areas of relatively open country
to be usable by condors and would have to include substantial areas
of adequate nest sites. They would have to be very large yet at the same
time be defensible from poachers.
A possible example of such an area is one that was considered
informally by the Recovery Team as an alternative to Hudson Ranch
during the crisis of 1985-1986-the Carrizo Plain of San Luis Obispo
County, California. This region is presently used almost exclusively for
ranching, and together with the associated Elkhorn Plain and the Cal-
iente Mountains, forms a well-defined geographic unit of importance
of a number of endangered species other than the condor. It is one of
the last strongholds for the San Joaquin kit fox (Vulpes macrotis mutica)
and the blunt-nosed leopard lizard (Crotophytus wislizenii silus). Fur-
thermore, it is an important wintering area for Sandhill Cranes and
Mountain Plover (Charadrius montanus), as well as for a variety of
raptor species, and it represents a potential reintroduction area for Tule
elk (Cervus nannodes), bighorn sheep (avis canadensis), and other
large mammals. Pronghorn (Antilocapra americana) have already been
reintroduced into this area.
While no known historic condor nest sites are located in this region,
it is within reasonable flying distance of the Sisquoc Sanctuary region
of Santa Barbara County; if condors could be successfully reestablished
in a subsidized population in the Sisquoc region, it would be well
worth considering the possibility of ultimately creating a mega preserve
linking the Carrizo Plain through the Cuyama Valley to the Sisquoc
region, repopulating this preserve with indigenous vertebrates, and fi-
nally converting the Sisquoc condor population from a subsidized pop-
ulation to one that feeds on indigenous vertebrates in the Carrizo Plain
and associated areas.
Certainly this would be an enormously expensive undertaking,
especially considering the necessity of controlling adequately large and
food-free buffer areas surrounding such a sanctuary, but it is not beyond
possibility. Much of the land involved is already federally owned, and

there are single philanthropists in this country well enough endowed
to underwrite purchase of the rest. In fact, movements toward acqui-
sition of large portions of this area are already underway by the Nature
Conservancy in cooperation with the BLM and the CDFG.
Another area with attractive potentials is the Gray Ranch region of
southwestern New Mexico. This region includes the Animas Mountains
and parts of the Peloncillo Mountains and vast acreages of grassland,
and like the Carrizo Plain, it offers habitat for a considerable number
of endangered species and species that could be potentially reintro-
duced, among them Aplomado Falcons (Falco femoralis) , Mexican wolves
(C. 1. baileyi), grizzly bears, Thick-billed Parrots (Rhynchopsitta pa-
chyrhyncha), pronghorns, bighorn sheep, bison (Bison bison), and many
unique amphibians, reptiles, and invertebrates. Pleistocene condor nests
are known from the region, and the many escarpments here offer nearly
unlimited potentials for future condor nest sites. Such a preserve might
be like an American Serengeti and could also be linked with additional
preserve acreage south of the Mexican border into an international park.
As very few people live in this area and land values are relatively low,
the expense of creating a mega preserve here could be considerably
lower than in the Carrizo Plain region, and the number of species ben-
efited other than the condor might potentially be considerably larger.
Regardless of where megapreserves might be established, they would
have to be surrounded by food-free buffer areas and maintained free of
hunting, if there is to be a reasonable chance that condors will survive
there. To this extent, the preserves should include ample numbers of
large predators, such as grizzlies, wolves, and cougar (Felis concolor),
to help regulate herbivore populations. The overall benefits of estab-
lishment of such preserves would far exceed the benefits to condors
alone.
5. DISCUSSION
Studies of the California Condor have always been hampered by

formidable practical difficulties. The species, while social at times in
roosting and feeding, has normally nested in dispersed distributions
and has often foraged and roosted solitarily. Long-range movements
and the inaccessibility of much of the species' habitat have made it
difficult to follow individuals. These characteristics have greatly hin-
dered efforts to census the species, to study reproduction, and to learn
very much about mortality factors. Researchers have had no choice but
CONDOR BIOLOGY AND CONSERVA TlON 255
to deal with the frustrations inherent in generalizing from incomplete

and biased data.
Many of the mistakes that have been made over the years have
stemmed from attempts to conclude too much from limited information.
Tentative hypotheses have evolved into "facts," more because of an
absence of competing hypotheses and a scarcity of data than because
of accumulation of supporting information, and researchers have found
themselves defending pronouncements based primarily on philosoph-
ical preferences and intuition. With only limited data available, it has
all too often been easy for ideas to gain acceptance simply on the basis
of perceived authority. Many outside observers presume, quite natu-
rally, that those studying the species are in especially favorable posi-
tions to evaluate data, and few outsiders take the trouble to examine
existing information critically and independently.
Thus, it has been easy for poorly substantiated ideas to become
established, whether they have concerned estimates of condor numbers,
conclusions about wariness and vulnerability of the species to distur-
bance, claims about whether the species has been breeding adequately,
or assertions as to what the most important mortality factors affecting
the species might be. These ideas have attracted more or less passionate
support, depending mainly on how persuasive their advocates have
been, and unfortunately have channeled conservation efforts in various
unproductive directions for many decades. Most regrettably, certain of
the ideas that have become established, i.e., those concerning sensitivity
of the species to interactions with man, have greatly hindered the very
process of getting better information on the problems faced by the spe-
cies. This specific difficulty is one that has also been faced in far too
many other endangered species programs.
Nevertheless, it is too easy to focus on the negative aspects of
condor research efforts and to forget that at the same time each of the
primary researchers has made important positive contributions. All
deserve respect for their accomplishments. It is impossible to study the
field records of the researchers involved with the species without de-
veloping a profound admiration for the efforts that have been made.
The important point to recognize is that while understanding has come
relatively slowly, definite progress has been made, and this progress
represents a synthesis of the efforts of many individuals. The basic
biology of the species is now well enough understood that conservation
strategies can be formulated with considerable confidence as to their
success.
The major gap in information that still exists is a comprehensive
understanding of the nature of the mortality factors causing the decline,
and it is on this subject that we feel weakest in generalizing. Although

we have emphasized the potential importance of lead poisoning, shoot-
ing, and collisions, the reader should not conclude that these factors
are the only ones of concern. Unfortunately, a fully comprehensive
evaluation of the mortality factors that have been responsible for the
decline is presently beyond reach, although presumably more will be
learned in the future with releases of captive condors to the wild.
It is our overall contention that the recent wild population of Cal-
ifornia Condors was probably doomed to extinction by the nature of
the threats it faced. As far as is known, these threats were entirely
human caused and in theory subject to human correction, but in prac-
ticality they were threats beyond correction in the time span available
and in the existing social and technological environment.
But this is not the end of the story. Assuming success in captive
breeding, we feel the chances are excellent that the species can be
returned successfully to the wild, but only under somewhat different
conditions than have prevailed in the recent natural range. The chal-
lenge is to find ways of doing this that are biologically, socially, and
economically viable. The "easy" part is to create subsidized popula-
tions in already secure habitats. The much harder part is to re-create
totally natural wild ecosystems large enough to sustain the species. We
recommend forgetting entirely about re-creating wild populhtions of
condors dependent on herds of domestic livestock and hunter-killed
wildlife. The political difficulties with this approach are likely to re-
main overwhelming into the indefinite future, and success in this ap-
proach could well wind up costing far more than re-creating totally
wild and natural ecosystems, which would be far preferable aestheti-
cally and biologically.
Regardless of what specific strategies may be followed in the future,
success can be expected to depend primarily on the quality of personnel
involved. In the past, the condor program has been fortunate to have
had the contributions of many very capable individuals and organi-
zations. But what has happened in the past is no guarantee of future
success unless mistakes of the past are well understood and efforts are
made to ensure that they will not be repeated. The extent to which the
program drifted away from biological and administrative soundness
during the crisis of 1985-1986 stands as a clear example of how easily
progress can be thrown away unless the people and organizations in-
volved remain cC'ntinuously concerned and vigilant. As details of the
1985-1986 crisis well illustrate a number of critical points re~arding
conduct and organization of endangered species conservation efforts,
we believe it is worthwhile taking a closer look here at certain of the

events and philosophies of this period.
One of the most puzzling developments during the crisis of
1985-1986 was the stance adopted by USFWS and NAS. In the face of
a catastrophic loss of 40% of the individuals and 80% of the breeding
potential of the wild population; in the face of strong recommendations
of population geneticists, many biologists, and the CFGC that the last
wild birds should be taken captive; and in spite of the fact that no
captive reproduction had yet been achieved; these organizations pro-
posed not only that six condors should be left in the wild but that three
of the existing captives should be turned loose.
Why did they make these proposals? Ostensibly it was an effort to
save habitat, preserve traditions of the wild population, maintain public
support for the program, and continue the effort to elucidate limiting
factors. But even the most elementary projections now indicated that
the mortality rate of the wild population was too high to preserve the
population for long, even by sacrificing some of the hard-won "capital"
then in captivity. In addition, the demographic and genetic adequacy
of the existing captive population was now in serious doubt, and there
was no longer any hope of achieving true adequacy by further multiple
clutching of wild pairs (only one remained). With the high mortality
rate of the wild population now standing in bold relief, why did it make
sense to the NAS and USFWS to preserve the traditions of the wild
population? And aside from Hudson Ranch, what habitat did NAS and
the USFWS want to save, when the USFS had taken pains to announce
that the Sespe and Sisquoc Sanctuaries, as well as all other nest sites
and roosts on National Forest lands, would continue to receive full
protection as long as there were reasonable prospects for reintroducing
condors into these areas in the future? Was it reasonable to expect more
habitat to be saved in the long run by watching the last condors die in
the wild than by creating a truly viable captive population capable of
supporting vigorous future release efforts? The official statements is-
sued by the USFWS and NAS to defend their proposal were not detailed
enough to give satisfactory answers to these questions and left many
observers skeptical as to whether the real reasons for the NAS-USFWS
proposal had yet surfaced.
It was many months before the main underlying reason for the
NAS-USFWS position emerged, and it was not one of the facile, but
basically unconvincing, justifications given in public statements. The
principal concern, as we eventually learned from conversations with
administrators of both organizations, was program preservation. Many
individuals in both organizations believed that it would be impossible

to maintain a condor field program if all condors were taken captive.
Loss of the field program carried a number of negative consequences.
Among other things, the jobs, security, power, and status of a sizeable
number of people were at stake, and not just people directly involved
with the field effort itself. By that time the annual USFWS-NAS budget
for the overall program was running over $1 million. Only a minority
of these dollars ever made their way out to the field program in Cali-
fornia. Even though leaving birds in the wild might well mean sacri-
ficing long-term chances for success in maintaining the species, the
short-term bureaucratic benefits of this approach were apparently com-
pelling. Further, the risks of this approach could be rationalized away
by faith in the capacity of the Hudson Ranch feeding program to keep
the wild birds alive.
Surprisingly, the program-preservation argument was also given
importance by some individuals outside the USFWS and NAS. In par-
ticular, the ADU Condor Committee, which met to consider the crisis
in May 1985, agreed that three or four condors should be left in the
wild, in large part to ensure continuation of the program. Apparently,
this committee was concerned that if the field program were to be
terminated, the expertise of personnel involved would be lost and that
starting up a new field program when releases became advisable at
some future date might be relatively difficult.
Was sacrifice of wild California Condors the only way to keep the
program going? Early in the crisis, we recommended that in addition
to bringing in the last wild birds, a program of surrogate releases of
Andean Condors should be instituted in the near term. Although the
Andean Condor release proposal was made primarily for biological
reasons, we pointed out that it also had political-bureaucratic benefits
in the sense of program preservation for those concerned about losing
programs, without any need for sacrifices of California Condors. How-
ever, neither the AOU Committee, the USFWS, the NAS, nor the Re-
covery Team was yet ready to embrace the Andean Condor release idea,
apparently believing it to have very limited political viability. So even
though the Andean Condor release proposal eventually came to be
favored by these organizations (when they found that it was in fact
politically viable), it was never perceived as a solution to the bureau-
cratic problem of program loss until long after the last wild condors
were well on their way to being trapped into captivity-another of the
many ironies of the condor program.
We were greatly troubled by the idea that short-term program pres-
ervation might be more important than giving captive breeding of the
condor the very best chance of success. We did not believe that if the
field program were to be discontinued there would be great difficulties
in gaining support for a reconstituted field effort for releases in the
future. And we did not believe it would be an insuperable task to find
well-qualified personnel to run that future effort. Were advocates of the
bird-sacrifice-to-save-programs approach really so confident that cap-
tive propagation might be fully successful with the limited genetic and
demographic base then in captivity? Captive breeding was now clearly
the only hope for preserving the species, yet it was still unknown how
many of the existing captives might prove to be breeders and how many
of these might produce genetically vigorous offspring. Overestimating
the captive breeding potentials of endangered species has never been
a wise practice.
Overall, we believe that one of the most important conclusions to
be drawn from the battles of 1985-1986 is that endangered species
bureaucracies are really no different from any other bureaucracies. They
follow the same immutable law of short-term self-interest, and this goal
tends to dominate all others. The tragedy of endangered species bur-
eaucracies is that in pursuing this goal they can force the species they
are charged with protecting to serve bureaucracy rather than the reverse.
In the case of the condor program, the instinct for bureaucratic self-
preservation was sufficiently strong that even by the late spring of 1986,
when the issue of bringing in the last wild birds had been settled
throughout the scientific community and at upper levels of the USFWS,
middle-level administrators of this organization, together with middle-
level administrators of NAS, were still drafting recommendations urg-
ing the leaving of some California Condors in the wild and the release
of captives to the wild in the near term, strategies that had lost essen-
tially all public support with the death of a lead-poisoned adult in
January 1986.
The upshot of the internal conflict within the USFWS over strat-
egies to be followed in condor conservation was that principal authority
for conduct of the program was removed from the chain of command
through the Patuxent Wildlife Research Center and the Research Di-
vision and was transferred to the regional director in Portland, Oregon,
in the spring of 1986. The regional director quickly appointed an ex-
cellent new Recovery Team for the species and announced that he
would develop condor policy based primarily on the recommendations
of this group, a refreshing change that returned the program at last to
a more reasonable biological and administrative foundation.
The condor program is now back to functioning on an open-forum
basis, with at least some administrators genuinely interested in input
from field biologists and with no one organization or minority of or-

ganizations having complete control over strategies. Although in some
respects a cumbersome way to operate, we believe it is ultimately the
best hope that the program may continue to move in basically positive
directions. The frustrations experienced by certain administrators of
the USFWS and NAS over not having unilateral control over the pro-
gram have been intense at times. Fortunately, their efforts in 1985-1986
to remove the program from an open forum and to move it in self-
serving directions contrary to sensible biology were unsuccessful.
The logical conclusion to draw from this experience is that there
is an overriding need for programs like the condor program to be guar-
nateed a free flow of information and biological expertise. Recovery
teams must be constituted with highly qualified personnel, i.e., mainly
field biologists, not administrators, and must be allowed to operate
without constraint. Something is very definitely wrong when the USFWS
forbids a recovery team to meet or constructs a recovery team without
competent biologists, as has happened on a number of occasions in
recent years. If the USFWS really wants to fulfill its obligations to the
taxpayer to preserve endangered species, it will hold these principles
to be of paramount importance.
In addition, there is a responsibility for administrators within or-
ganizations such as the USFWS and NAS to first of all place highly
competent researchers in the field and then to respect and follow their
recommendations. Without a firm foundation of good biology, nothing
can possibly be achieved. Organizations must resist the temptations to
hire field biologists for their bureaucratic malleability rather than their
biological research capacities. "Team players" rarely make good biol-
ogists, and attempts to run endangered species programs in top-down
military fashion cannot succeed.
We bring up these points because they are of the utmost impor-
tance, because there are strong forces operating in other directions within
all bureaucracies, and because in many instances there have been fla-
grant deviations from these principles. Successful endangered species
programs unfortunately do not just happen. They have to be fought for
in many ways that are totally invisible to the public and can be quickly
scuttled by bureaucratic expediency.
When the modern condor program was initiated in 1980, we our-
selves were frustrated by the fact that so many public and private agen-
cies and individuals were involved and because it appeared unlikely
that a consensus would ever develop on any issue. The fact that both
federal and state permission had to be gained for all major actions
seemed especially unwidely and unnecessary. However, the perspec-
CONDOR BIOLOGY AND CONSERVATION 21;1
tive gained with a number of years experience in working under such

a system is that the crucial advantages of shared power, combined with
open free discussions, far outweigh the disadvantages. If conservation
strategies are fundamentally wise, practical, and needed, the chances
are good under such a system that they will ultimately be given a fair
hearing and will be implemented. Poorly conceived, self-serving, and
expedient strategies will probably not long survive, as long as the de-
cision-makers on the whole are sincerely committed to the goals they
are charged to uphold by the public.
We remain optimistic about ultimate success in condor conser-
vation precisely because of the high degree of general public interest
and involvement that has characterized the program. Without the bal-
ance this involvement gives, the program could very easily drift into
invisible bureaucratic stagnation and retrogression. Government agen-
cies very definitely need to be watched closely to ensure that they fulfill
their obligations. Private agencies are not intrinsically any better, and
in fact they can often better conceal their actions and motives from the
public. Thus, we believe that the best hope for success lies in the
interplay of a diversity of interests, in maintenance of a truly open
forum for discussions, and in continued involvement of highly qualified
researchers at the field level. These are all difficult considerations,
especially in the long haul.
One final point we believe to be worth emphasizing is that only
under extremely unusual conditions do nonintensive approaches to
conservation of critically endangered species make any sense. The prob-
lems faced by endangered species are often relatively complicated, and
it is essential that these threats be thoroughly understood, if conser-
vation efforts are to be successful. Without intensive research and con-
servation approaches, the California Condor would now be lost, as
would the Puerto Rican Parrot, the Bermuda Petrel (Pterodroma cahow),
and a number of other species. Similarly, without intensive research,
the overwhelming threat posed to native Hawaiian birds by avian dis-
eases would still be unknown. One does not conserve species suffering
from avian diseases by saving habitat (not that they do not need habitat
too), and one does not conserve populations threatened by lead poi-
soning by stopping 1080 poisoning. Unfortunately, it is an almost uni-
versal characteristic of bureaucracies to be reluctant to allow intensive
research and conservation efforts with endangered species, for fear that
something might go wrong and for fear of opposition from organizations
and individuals that are basically anti-research and are content with
unsubstantiated guesses as to what the problems of endangered species
might be. Intensive research and conservation efforts do carry risks, but
far more often than not these risks pale in comparison with the risks
of pursuing ineffective and ill-advised conservation remedies. In the
long run, the abilities of endangered species programs to command
support from the public will stand in direct proportion to their success,
which in turn will rarely be achieved without sound biological under-
standing.
ACKNOWLEDGMENTS. The condor program has been a sometimes co-

operative, sometimes not so cooperative, venture of many individuals
and organizations, all of whom deserve acknowledgment for their con-
tributions. Unfortunately, the number of contributors is so large that it
would be impractical to mention them all, and we will limit ourselves
to major contributors to the modern program. Primary institutional
support over the years has come from the U. S. Fish and Wildlife
Service, the National Audubon Society, the U. S. Forest Service, and
the California Department of Fish and Game; but in recent years sub-
stantial support has also come from the Bureau of Land Management,
the San Diego and Los Angeles Zoos, the Condor Survival Fund, Hawk
Mountain Sanctuary Association, the Biological Sciences Department
of California Polytechnic State University at San Luis Obispo, the Santa
Barbara Museum of Natural History, the Western Foundation of Ver-
tebrate Zoology, the Illinois Natural History Survey, the Santa Cruz
Predatory Bird Research Group, the Los Angeles, Morro Coast, Kern,
Santa Barbara, and Tulare County Audubon Societies, the Hearst Foun-
dation, and Van Nuys Charities. This chapter, however, should not be
considered an official expression of the viewpoint of any particular
organization. It is our own personal assessment of the biology and
conservation of the species.
Nevertheless, while we have used the pronoun "we" throughout
the chapter, the reader should recognize that especially with regard to
results of studies in the modern program "we" generally refers in large
measure to the efforts of a remarkable staff of assistants and cooperators.
In particular, we wish to acknowledge the following field assistants,
who worked closely with us in the part of the program we supervised:
Louis Andaloro, Victor Apanius, Lee Aulman, Brad Bush, Dave Clen-
denen, Jan and Hank Hamber, Leon Hecht, Jack Ingram, Dave Ledig,
Cindy McConathy, Teresa Nichols, Sandy Pletschet, Rob Ramey, John
Roach, Bay Roberts, John Roser, Joe Russin, John Schmitt, Meg Stein,
and Russell Thorstrom. These individuals worked exceptionally hard
and were responsible for a major portion of the achievements of the
modern program.
We have also drawn on some of the results of the condor radio-
telemetry program run primarily by John Ogden and his staff consisting
of Bruce Barbour, Peter Bloom, Jesse Grantham, Vicky Meretsky, Larry
Riopelle, Greg Sanders, and Buck Woods. Other staff members of the
CRC who have made important contributions are Gary Falxa, Steve
Kimple, William Lehman, and Cindy Studer.
Special acknowledgment should be given to personnel of the San
Diego and Los Angeles Zoos, who have aided the program in many
ways transcending captive breeding of condors. In particular, mention
must be made of Jack Allen, Marilyn Anderson, Cathleen Cox, Mike
Cunningham, Phil Ensley, Ben Gonzalez, Marcia Hobbs, Don Janssen,
Cyndi Kuehler, Gary Kuehn, Arlene Kumamoto, Don Lindburg, Mike
Loomis, Jim Oosterhuis, Art Risser, Amy Shima, Don Sterner, Warren
Thomas, Bill Toone, Rebecca Usnik, Mike Wallace, and Pat Witman for
their many contributions. Eric Johnson and his students at California
Polytechnic State University made crucial contributions with respect
to censusing of the wild population.
Members of the various Condor Recovery Teams deserve special
ackowledgment for consistently placing the welfare of the species over
the biases of their respective organizations in charting overall strategies
for the program.
We are especially grateful to Rod Drewien, Eric Johnson, Lloyd
Kiff, Fred Sibley, and Mike Wallace for offering comments on portions
or all of various drafts of the manuscript. And finally, we wish to make
special acknowledgment of the important role of Mike Wallace in con-
ducting release experiments with surrogate species and in developing
strategies for future releases of captive California Condors to the wild.
Much of what we have presented on this subject derives from his rec-
ommendations.
The number of people who have contributed significantly to con-
servation of the condor is far greater than these brief and incomplete
acknowledgments might suggest. If the condor does survive its perilous
condition, this will be the most fitting acknowledgment of all these
efforts.
REFERENCES
Anonymous, 1985, Audubon action alert, August 2, 1985, National Audubon Society,
Washington, D. C.
Borneman, J. c., 1966, Return of a condor, Audubon Mag. 68:154-157.
Brown, W. M., Drewien, R. C., and Bizeau, E. G., 1987, Mortality of cranes and waterfowl
from power line collisions in the San Luis Valley, Colorado, in: Proceedings of the
1985 Crane Workshop (J. C. Lewis, ed.), Platte River Whooping Crane Habitat Main-
tenance Trust and U. S. Fish and Wildlife Service, Grand Island, Nebraska, pp.
128-136.
Carpenter, J. W'O 1982, Medical and husbandry aspects of captive Andean Condors: A
model for the California Condor, in: Annual Proceedings of the American Association
of Zoo Veterinarians, 1983, pp. 13-19.
Carrier, W. D., 1971, Habitat management plans for the California Condor, U.S. Forest
Service.
Dana, R. H., 1840, Two Years before the Mast, Harper, New York.
Decker, R. A., McDermid, A. M., and Prideaux, J. W., 1979, Lead poisoning in two captive
King Vultures, J. Am. Vet. Med. Assoc. 175:1009.
Elveru, 1., 1983, A reprieve for the condor, Swarthmore Call. Bull. 80:2-5.
Emslie, S. D., 1987, Age and diet of fossil California Condors in Grand Canyon, Arizona,
Science 237:768-770.
Faanes, C. A., 1987, Bird behavior and mortality in relation to power lines in prairie
habitats. USDI Fish Wildl. Servo Tech. Rep. No.7, Washington D. C.
Finley, W. 1., 1906, Life history of the California Condor. I. Finding a condor's nest,
Condor 8:135-142.
Finley, W. L., 1908a, Life history of the California Condor. II. Historical data and range
of the condor, Condor 10:5-10.
Finley, W. L., 1908b, Life history of the California Condor. III. Home life of the condor,
Condor 10:59-65.
Finley, W. 1., 1908c, Home life of the California Condor, Century 75:370-380.
Finley, W. L., 1908d, California Condor, Sci. Am. 99:7-8.
Finley, W. 1., 1909, General, a pet California Condor, Ctry Life 16:35-38.
Finley, W. 1., 1910, Life history of the California Condor. IV. The young condor in
captivity, Condor 12:5-11.
Finley, W. L., and Finley, I., 1915, Condor as a pet, Bird-lore 17:413-419.
Finley, W. L., and Finley, I., 1926, Passing of the California Condor, Nat. Mag. 8:95-99.
Garcelon, D. K., Risebrough, R. W., and Jarman, W. M., 1988, Reintroduction of Bald
Eagles to Santa Catalina Island in southern California, in: Proceedings of the Third
World Conference on Birds of Prey (R. B. Chancellor, ed.), ICBP, London, in press.
Gilmartin, W. G., DeLong, R. 1., Smith, A. W., Sweeney, J. c., de Lappe, B. W., Risebrough,
R. W., Griner, L. A., Dailey, M. D., and Peakall, D. B., 1976, Premature parturition
in California sea lions, J. Wildl. Dis. 12:104-115.
Harris, H., 1941, The annals of Gymnogyps to 1900, Condor 43:3-55.
Harrison, E. N., and Kiff, L. F., 1980, Apparent replacement clutch laid by wild California
Condor, Condor 82:351-352.
Hegdahl, P. 1., Gatz, T. A., Fagerston, K. A., Glahn, J. F., and Matschke, G. H., 1979,
Hazards to wildlife associated with 1080 baiting for California ground squirrels.
Final Report on Interagency Agreement EPA-IAG-07-0449, U. S. Fish and Wildlife
Service, Environmental Protection Agency, Washington, D. C.
Jackson, J. A., 1983, Nesting phenology, nest site selection, and reproductive success of
Black and Turkey Vultures, in: Vulture Biology and Management (S. R. Wilbur and
J. A. Jackson, eds.), University of California Press, Berkeley and Los Angeles, pp.
245-270.
Janssen, D. 1., Oosterhuis, J. E., Allen, J. L., Anderson, M. P., Kelts, D. G., and Wiemeyer,
S. N., 1986, Lead poisoning in free-ranging California Condors, J. Am. Vet. Med.
Assoc. 155:1052-1056.
Johnson. E. V .. 1985. Commentary. California Condor population estimates. Condor

87:446-447.
Johnson. E. V .. Aulman. D. L.. Clendenen. D. A .. Guliasi. G .. Morton. L. M .• Principe. P.
I.. and Wegener. G. M .. 1983. California Condor: Activity patterns and age compo-
sition in a foraging area. Am. Birds 37:941-945.
Jurek. R.. 1983. Chronology of significant events in California Condor history. Outdoor
Calif. 44:42.
Kiff. L.. 1983. An historical perspective on the condor. Outdoor Calif. 44:5-6. 34-37.
Kiff. L. F .. Peakall. D. B.. and Wilbur. S. R.. 1979. Recent changes in California Condor
eggshells. Condor 81:166-172.
Koford. C. B.. 1950. The natural history of the California Condor (Gymnogyps califor-
nianus). doctoral dissertation. University of California. Berkeley.
Koford. C. B.. 1953. The California Condor. Nati. Audubon Soc. Res. Report No. 4:1-154.
Kuehler. c.. and Witman. P. N .. 1988. Artificial incubation of California Condor (Gym-
nogyps californianus) eggs removed from the wild. Zoo BioI.. 7:123-132.
Latta. F. F .. 1976. Saga of Rancho el Tej6n. Bear State Books. Santa Cruz.
Locke. L. N .. Bagley. G. E.. Frickie. D. N .. and Young. L. T .. 1969. Lead poisoning and
aspergillosis in an Andean Condor. ,. Am. Vet. Med. Assoc. 155:1052-1056.
Mallette. R. D .. 1970. Operational Management Plan for California Condor. California
Department of Fish and Game. Sacramento.
Mallette. R. D.. and Borneman. J. c.. 1966. First cooperative survey of the California
Condor. Calif. Fish Game 52:185-203.
McMillan. E.. 1981. Interview. spring 1980. in The Condor Question. Captive or Forever
Free? (D. Phillips and H. Nash. eds.). Friends of the Earth. San Francisco. pp. 139-156.
McMillan. I.. 1953. Condors. politics and game management. Central Calif. Sportsm(]n.
repr. from December issue. 13(12):458-460.
McMillan. I.. 1968. M(]n and the California Condor. Dutton. New York.
McMillan. I.. 1970. Botching the condor program. Defenders Wildi. News 45:95-98.
McMillan. I.. 1971. The 1971 condor survey-A return to soundness. Defenders Wildi.
News 46:386.
McMillan. I.. 1981. Interview. spring 1980. in: The Condor Question. Captive or Forever
Free? (D. Phillips and H. Nash. eds.). Friends of the Earth. San Francisco. pp. 121-131.
Mead. P. S .. Morton. M. L.. and Fish. B. E.. 1987. Sexual dimorphism in egg size and
implications regarding facultative manipulations of sex in Mountain White-crowned
Sparrows. Condor 89:798-803.
Miller. A. H .. 1953. The case against trapping California Condors. Audubon Mog.
55:261-262.
Miller. A. H .. McMillan. I.. and McMillan. E.. 1965. The current status and welfare of
the California Condor. Nati. Audubon Soc. Res. Report No. 6:1-61.
Mundy. P. J.. 1982. The Comp(]rative Biology of Southern Afric(]n Vultures. Vulture
Study Group. Johannesburg.
Olendorff. R. R.. and Lehman. R. N .. 1~l86. Raptor collisions with utility lines: An analysis
using subjective field observations. Final report. U. S. Dept. of Interior to Pacific Gas
and Electric Company. San Ramon. California.
Phillips. 0 .. and Nash. H. (eds.). 1981. The Condor Question. Captive or Forever Free'!
Friends of the Earth. San Francisco.
Rea. A. M .. 1981. California Condor captive breeding: A recovery proposal. Environ. SW
484:8-12.
Ricklefs, R. E. (ed.), 1978, Report of the advisory panel on the California Condor, Natl.
Audubon Soc. Conserv. Report 6:1-27.
Risser, A. C., Jr., 1983, What about third condor egg?, Zoonooz 56:14-15.
Robinson, C. S., 1936a, A report on study of life habits of the California Condor, U. S.
Forest Service, Santa Barbara.
Robinson, C. S., 1936b, Protection of the California Condor, U. S. Forest Service, Santa
Barbara.
Robinson, C. S., 1939, Observations and notes on the California Condor from data col-
lected on Los Padres National Forest, U. S. Forest Service, Santa Barbara.
Robinson, C. S., 1940, Notes on the California Condor, collected on Los Padres National
Forest, California, U. S. Forest Service, Santa Barbara.
Schafer, H. A., Gossett, R. W., Ward, C. F., and Westcott, A. M., 1984, Chlorinated
hydrocarbons in marine mammals, in: Southern California Coastal Water Research
Project, Biennial Report, 1983-84 (W. Bascom, ed.). Southern California Coastal
Water Research Project, Long Beach, pp. 109-114.
Sibley, F. C., 1969, Effects of the Sespe Creek Project on the California Condor, U. S.
Fish and Wild!. Serv., Laurel, Maryland.
Snyder, N. F. R., 1983, California Condor reproduction, past and present, Bird Conserv.
1:67-86.
Snyder, N. F. R., 1986, California Condor recovery program, in: Raptor Research Report
No.5: Raptor Conservation in the Next 50 Years (S. E. Senner, C. M. White, and
J. R. Parrish, eds.), Raptor Research Foundation, pp. 56-71.
Snyder, N. F. R., and Hamber J. A., 1985, Replacement-clutching and annual nesting of
California Condors, Condor 87:374-378.
Snyder, N. F. R., and Johnson, E. V., 1985a, Photographic censusing of the 1982-1983
California Condor population, Condor 87:1-13.
Snyder, N. F. R., and Johnson, E. V., 1985b, Photos key to condor census, Outdoor Calif.
46:22-25.
Snyder, N. F. R., Johnson, E. V., and Clendenen, D. A., 1987, Primary molt of California
Condors, Condor 89:468-485.
Snyder, N. F. R., Ramey, R. R., and Sibley, F. C., 1986, Nest-site biology of the California
Condor, Condor 88:228-241.
Snyder, N. F. R., Wiley, J. W., and Kepler, C. B., 1987, The Parrots of Luquillo: Natural
History and Conservation of the Puerto Rican Parrot, Western Foundation of Ver-
tebrate Zoology, Los Angeles.
Stager, K., 1964, The role of olfaction in food location by the Turkey Vulture (Cathartes
aura), LA City Mus. Contrib. Sci. 81:1-63.
Studer, C. D., 1983, Effects of Kern County cattle ranching on California Condor habitat,
Master's thesis, Michigan State University, East Lansing.
Terrasse, M., 1985, Reintroduction du Vautour Fauve dans les Grands Causses (Cevennes).
Fonds d'Intervention pour les Rapaces.
U. S. Fish and Wildlife Service, 1975, California Condor Recovery Plan, Washington,
D. C., approved April 9, 1975, 63 pp.
Verner, J., 1978, California Condors: status of the recovery effort, Gen. Tech. Rep. PSW-
28, U. S. Forest Serv., Washington, D. C.
Wallace, M. P., and Temple, S. A., 1983, An evaluation of techniques for releasing hand-
reared vultures to the wild, in: Vulture Biology and Management (S. R. Wilbur and
J. A. Jackson, eds.), University of California Press, Berkeley and Los Angeles, pp.
400-423.
Wallace, M. P., and Temple, S. A., 1987, Releasing captive-reared Andean Condors to
the wild, J. Wildl. Mgmt. 51:541-550.
Wiemeyer, S. N., Jurek, R M., and Moore, J. R, 1986, Environmental contaminants in
surrogates, foods, and feathers of California Condors (Gymnogyps californianusJ,
Environ. Monit. Assess. 6:91-111.
Wiemeyer, S. N., Krynitsky, A. J., and Wilbur, S. R, 1983, Environmental contaminants
in tissues, foods, and feces of California Condors, in: Vulture Biology and Manage-
ment (S. R Wilbur and J. A. Jackson, eds.), University of California Press, Berkeley
and Los Angeles, pp. 427-439.
Wiemeyer, S. N., Scott, J. M., Anderson, M. P., Bloom, P. H., and Stafford, C. J., 1988,
Environmental contaminants in California Condors, J. Wildl. Mgmt. 52:238-247.
Wilbur, S. R., 1977, Supplemental feeding of California Condors, in: Endangered Birds,
Management Techniques for Preserving Threatened Species (S. A. Temple, ed.),
University of Wisconsin Press, Madison, pp. 135-140.
Wilbur, S. R, 1978, The California Condor, 1966-76: A look at its past and future, U. S.
Fish Wildl. Servo North Am. Fauna 72:1-136.
Wilbur, S. R, 1980, Estimating the size and trend of the California Condor population,
1965-1978, Calif. Fish Game 66:40-48.
Wilbur, S. R, Carrier, W. D., and Borneman, J. C., 1974, Supplemental feeding program
for California Condors, J. Wildl. Mgmt. 38:343-346.
CHAPTER 6
OLFACTORY ORIENTATION BY
BIRDS
JERRY A. WALDVOGEL
1. INTRODUCTION
An animal's ability to orient effectively within and between suitable

habitats is a matter crucial to survival. Birds, being extremely mobile
creatures with high metabolic demands, are more dependent than most
vertebrates on successful movements that maximize their utilization of
environmental resources. Whether these movements are short flights
necessary for the maintenance of a territory, longer foraging trips that
may cover many kilometers, or truly long-distance migrations of trans-
continental proportions, the need for accurate information about po-
sition and direction is fundamental to a bird's survival and reproductive
success. Exactly how birds use the environmental cues that provide
this information has been a subject of study for several decades, al-
though our knowledge of the mechanisms that control avian orientation
behavior remains far from complete.
Many environmental phenomena have received attention as can-
didates for the physical cues upon which avian orientation is based.
These include the motion of celestial bodies such as the sun or the
stars, patterns of directional variation in the earth's geomagnetic and
JERRY A. WALDVOGEL· Section of Neurobiology and Behavior. Cornell University,

Ithaca, New York 14853.
26(1
270 JERRY A. WALDVOGEL
gravitational fields, acoustic characteristics of certain atmospheric phe-

nomena, and naturally occurring olfactory cues (reviewed by Keeton,
1974a; Emlen, 1975; Able, 1980; Papi, 1986; Schmidt-Koenig, 1987).
Among these, perhaps the most surprising suggestion involves the pos-
sibility that birds use odors as a source of directional information. At
first glance, the small size of the olfactory lobes in the avian forebrain
gives the impression that birds lack the sensory processing mechanisms
needed for a detailed analysis of environmental odors. Indeed, of the
five basic senses common to all vertebrates, olfaction has traditionally
been considered the least well developed in birds. Theoretical argu-
ments against the existence of stable atmospheric olfactory cues have
also tended to foster the view that olfaction plays only a minor role in
the day-to-day behavior of birds.
Such a priori antiolfactory biases in the study of bird behavior are
now giving way to the realization that most (if not all) birds possess a
functional sense of smell (Bang and Wenzel, 1985). However, because
this change has corne about only recently, research into olfactory in-
fluences on bird behavior has also only just begun in earnest. One line
of research with a good head start is the study of avian olfactory ori-
entation, due primarily to the large number of experiments which have
examined the possibility of olfactory navigation by homing pigeons,
Columba livia (reviewed by Papi, 1986; Schmidt-Koenig, 1987). But
even within this area of research, conflicting opinions exist regarding
the interpretation of results from olfactory orientation experiments (e.g.,
Papi et 01., 1978a; Gould, 1982a; Papi, 1982; Wallraff, 1982, in response
to Gould). One problem in these discussions has been a failure to ap-
preciate fully the present extent of our knowledge about avian olfactory
capabilities. In addition, there has been a failure to consider important
physical factors, such as the role of atmospheric dynamics in odor
dispersion. An unfortunate outcome has been the overshadowing of
data that clearly demonstrate some level of olfactory orientation by
species other than pigeons. Since many ornithologists will have read
or heard only about influences on olfactory orientation in pigeons, it
is my purpose here to review the evidence that now exists both for and
against the use of odors by all birds. Wherever possible, an analysis of
relevant physiological, atmospheric, and behavioral considerations is
included. In order to accomplish this, the evidence regarding avian
olfactory sensitivity, as well as the physical mechanisms affecting odor
transport in the atmosphere, are also briefly reviewed. In the process,
I hope to illustrate the limits of our understanding about avian olfactory
orientation and thereby build a useful framework for guiding future
research.
OLF ACTORY ORIENT ATION 271
2. TYPES OF ORIENTATION
The possible orientation strategies used by birds and other animals

can be classified into three basic categories (Griffin, 1955). The first,
known as piloting by landmarks, involves orientation using memory-
based relationships among relatively stationary environmental cues.
These landmark cues can take many forms. Humans, for instance, rely
primarily on visual landmarks for orientation, as evidenced by our
tendency to give directions in terms of colors, shapes, and familiar
objects. There is also good evidence that many other organisms, in-
cluding birds, utilize visual landmarks for orientation (Schone, 1984).
But nonvisual sensory systems such as echolocation and olfaction may
also be used to obtain landmark information. For example, many mam-
mals rely heavily on olfactory cues associated with their feces or urine
to create odor landmarks which denote territorial boundaries. Natural
odor landmarks are also used as orientation cues in foraging, with
several species of procellariiform birds among the best known exam-
ples. Additional examples of avian orientation by means of olfactory
landmarks are presented in Section 5.1.
A second type of orientation involves the maintenance of a compass
heading over long distances, independent of familiar landmarks. All
compasses require access to some geophysical parameter capable of
providing accurate directional information, except in the case of an
idiothetic compass that functions by integrating previous motion to
arrive at a compass direction (Schone, 1984). Known geophysical sources
of compass information include the sun, the stars, patterns of natural
polarized skylight, and the earth's magnetic field (Keeton, 1974a; Able,
1980). Compass orientation strategies are common among many groups
of animals, and are especially well developed in migratory birds. The
possibility that olfaction might act as a reliable compass cue in bird
orientation is the topic of Section 5.2.
The third type of orientation, commonly referred to as map and
compass orientation or true navigation, involves a two-step process
analogous to the use of a map and compass by human navigators. The
first step requires a position fix, during which the animal determines
its current position relative to a chosen goal by means of a "map sense."
Once a goalward direction has been ascertained using the navigational
map, the animal then employs one of several possible compass mech-
anisms to determine the correct direction of travel. True navigation is
probably quite common among birds. For example, many temperate
zone birds tend to return to the same nesting site in successive years.
These long-distance migrants are likely using true navigation during
the final phase of their journey, if not throughout (Able, 1980). Homing
pigeons are also thought to employ true navigation when rapidly finding
their way home from distances of hundreds of kilometers through un-
familiar territory; suggestions that olfactory navigation may guide this
behavior provide but one of several possible explanations for the mech-
anism involved (Papi, 1976; 1986). Section 5.3 discusses the evidence
for olfactory navigation in birds. However, before undertaking a be-
havioral analysis of avian olfactory orientation, it is necessary to con-
sider the sensory constraints placed on each of Griffin's three orien-
tation strategies by virtue of the physiological limits that define olfactory
sensitivity in birds.
3. AVIAN OLFACTORY SENSITIVITY
When compared to other classes of vertebrates, birds are generally

considered microsmotic. This designation is based not only on an ap-
parent lack of behaviors that are obviously guided by olfaction, but also
on the small size of avian olfactory neural tissue and its relatively low
level of complexity. This anatomical view that birds are olfactorially
inferior to such obviously macrosmotic vertebrates as fish and mammals
has tended to reinforce a priori beliefs that olfaction does not greatly
influence avian behavior and is in large part responsible for a general
lack of research on the topic of odor perception by birds. However, as
Stoddart (1980) points out, the terms microsmotic and macrosmotic can
be misleading because they give no impression of specialized sensitivity
to one or a group of odorants for which a structurally small system may
have evolved. Despite this cautionary note, the view that birds uni-
formly possess a poorly developed sense of smell has only recently
begun to yield in the face of experimental evidence to the contrary.
First among the proponents of a revised view of avian olfaction
were numerous nineteenth and twentieth century anatomists, who pro-
vided us with a rather complete understanding of the often complex
olfactory anatomy in birds. Since this work was recently reviewed (Bang
and Wenzel, 1985), it is not discussed here. This section concentrates
instead on early efforts to assess avian olfactory sensitivity in the lab-
oratory, later successes at comparing patterns of avian olfactory anat-
omy with the behavioral and ecological tendencies exhibited by diverse
bird groups, and more recent laboratory measurements of avian olfac-
tory thresholds that clearly demonstrate a functional sense of smell.
OLFACTORY ORrENTATION 273
3.1. Early Attempts to Study Avian Olfaction

Suggestions that olfaction might function as more than a remnant
sensory system in birds date back to the last century (Owen, 1872;
Parker, 1891). Nevertheless, the structure-function relationships that
emerged from these purely anatomical observations have until very
recently remained a matter of conjecture. Indeed, the earliest attempts
at olfactory conditioning experiments by Strong (1911) and Walter (1943)
failed to establish conditioned reflexes that would permit an evaluation
of olfactory capabilities in such species as pigeons, ducks, and para-
keets. Despite this negative evidence, both Strong and Walter suggested
that their failure to demonstrate olfactory detection in birds behavior-
ally likely resulted from inadequate technical sophistication regarding
the manipulation of odors. They therefore cautioned that their work
was not a definitive statement on the presence or absence of olfactory
sensitivity in birds. This unwillingness to embrace negative evidence
as proof was rewarded when Michelsen (1959), using advancements in
behavioral training and odor-handling techniques, succeeded in con-
ditioning pigeons to respond to the laboratory chemical odorant iso-
octane, signaling the start of modern work on olfactory sensitivity in
birds.
Shortly after Michelsen's experiments were published, Bang and
Cobb presented a series of papers that surveyed dozens of bird species
from most avian orders in an effort to associate the anatomical extent
of a bird's olfactory apparatus with its particular ecological character-
istics (Bang, 1960, 1971; Cobb, 1960a,b; Bang and Cobb, 1968). These
analyses show that birds with the largest olfactory ratio (expressed as
the ratio between the longest diameter of the olfactory bulb and the
longest diameter of the ipsilateral cerebral hemisphere) could generally
be categorized as ground-nesting, water-associated, colonial breeders
that were also primarily carnivorous (especially pisicivorous). Exam-
ples of avian groups with large olfactory ratios (>25%) include many
of the procellariids (e.g., petrels, shearwaters, and fulmars), some spe-
cies of vultures, kiwis, and the oilbird. Conversely, species with small
olfactory ratios «15%) are typically categorized as tree-nesting, land-
living, granivorous and solitary in their breeding habits. Examples in-
clude many of the passerines, the corvids, and most gallinaceous birds.
Other avian groups, such as the pigeons, waterfowl, and raptors, have
intermediate olfactory ratios (15-25%) and exhibit a mixture of the
ecological and behavioral characteristics cited above. Since the time of
Bang and Cobb's anatomical/ecological analysis, numerous physiolog-
ical and behavioral studies have demonstrated conclusively that chem-
ical odorants do evoke a definite response in avian olfactory tissue

(reviewed by Bang and Wenzel, 1985) and that the species with the
best olfactory responses appear to be, with some exceptions, those with
the highest olfactory ratios (see Section 5.1.1).
3.2. Olfactory Thresholds

Unfortunately, correlations between characteristics of olfactory
anatomy and the behavioral ecology of specific bird groups do not tell
us much about how the avian olfactory system actually works. To obtain
this kind of information about sensory perception, controlled experi-
ments must be conducted in which known concentrations of olfactory
stimuli are presented to birds while changes in a reliable physiological
response are noted. In the few tests in which the reaction of some
continuous physiological process (e.g., olfactory bulb electrical activity,
heart rate, or respiration rate) has been monitored with respect to the
presence of an olfactory stimulus, good evidence for odor perception
has been obtained for every species of bird tested, irrespective of ol-
factory bulb size (e.g., Neuhaus, 1963; Wenzel, 1967; Wenzel and Sieck,
1972; Macadar et al., 1980; Walker et al., 1986). In addition, a clear
behavioral response to odors has been demonstrated during the late
stages of development in unhatched embryos of the domestic chicken
(Gallus gallus), showing that a functional sense of smell exists in at
least some birds, beginning at hatching (Tolhurst and Vince, 1976).
Despite the indications that many if not all birds possess a func-
tional olfactory sense, only five species have ever actually been tested
for absolute or differential olfactory thresholds (Table I). This paucity
of olfactory sensitivity data is particularly frustrating because it forces
us to make broad generalizations about avian olfaction on the basis of
an extremely limited sampling of species. Moreover, the odors that have
commonly been used in such experiments are often of questionable
biological relevance to the species tested. Thus, for example, such stan-
dard laboratory chemicals as benzaldehyde, hexane, n-amyl acetate,
and pentane have been used to show that the absolute olfactory thresh-
old for pigeons (as determined by operant and cardiac conditioning
techniques) ranges from 0.1 to 20 x 10- 6 M (Henton, 1969; Shumake
et aJ., 1969; Walker et aJ., 1986). That this detection is based on olfaction
and not some other chemical sense is shown by the significant increase
in threshold concentration required to successfully stimulate pigeons
whose olfactory nerves have been bilaterally resected (Walker et aJ.,
1986). By comparison, absolute sensitivity thresholds to certain chem-
icals are known to range from 10 -14 M in eels and dogs (Teichman,
OLFACTORY ORIENTATION 275
TABLE I
Absolute Olfactory Sensitivity Thresholds for Five Species of Birds
Threshold conc.
Species Odorant tested (x 10- 6 M}a Reference
Pigeon Benzaldehyde 0.6 Walker et a1. (1986)
(Columba livia) Butanol 0.8 Walker et a1. (1986)
Butanethiol 600 Snyder and Peterson (1979)
Ethanethiol 1000 Snyder and Peterson (1979)
Heptane 0.3 Stattleman et a1. (1975)
Hexane 2.0 Stattleman et a1. (1975)
Menthol 0.8 Snyder and Peterson (1979)
n-Amyl acetate 0.5 Walker et al. (1986)
n-Butyl acetate 0.2 Walker et a1. (1986)
Pentane 18 Stattleman et a1. (1975)
Domestic chicken Heptane 0.5 Stattleman et a1. (1975)
(Gallus gallus) Hexane 0.8 Stattleman et a1. (1975)
Pentane 1.7 Stattleman et a1. (1975)
Bobwhite quail Heptane 2.5 Stattleman et a1. (1975)
(Colinus Hexane 3.8 Stattleman et a1. (1975)
virginianus) Pentane 9.0 Stattleman et a1. (1975)
Black-billed magpie Butanethiol 500 Snyder and Peterson (1979)
(Pica pica) Ethanethiol 800 Snyder and Peterson (1979)
Menthol 1.5 Snyder and Peterson (1979)
Turkey vulture Butanoic acid 1.0 Smith and Paselk (1986)
(Cathartes aura) Ethanethiol 1.0 Smith and Paselk (1986)
Trimethylamine 10 Smith and Paselk (1986)
"For ease of comparison. all threshold sensitivities are given as molar 1M) concentrations of the odorant
necessary to evoke a criterion olfactory response. regardless of the units in which the data were
originally published. This has required some averaging of data and their conversion from other units
such as percentage saturation. parts per thousand (ppt). parts per million (ppm). or parts per billion
(ppb). which are also commonly used in the literature. Note that 10.- 3 M = 1 ppt. 10 -Ii M =
1 ppm. and that 10-'1 M = 1 ppb.
1959) to 10- 9 M in man (Wright, 1964). Amyl acetate, which can be

detected by pigeons in concentrations of 10- 6 M, is sensed by rats at
concentrations as low as 10- 18 M (Davis, 1973). Unfortunately, direct
comparisons of olfactory sensitivity among vertebrate species is often
misleading given the potential for an animal to specialize in the de-
tection of a few odors only. Thus, for example, salmon are extremely
sensitive to certain amino acid compounds normally found in the water
of their natal stream, detecting these substances at concentrations of
10 - 9 M, while at the same time they are essentially oblivious to the
many other organic chemicals present in much higher concentrations
but which apparently lack meaning as identifiers of the home river
system (Hara, 1975). Therefore, it appears that the best conclusion by
way of comparison is that pigeons, and perhaps all birds, are on the
lower (Le., less capable) end of the spectrum of vertebrate olfactory
sensitivity.
Within the class Aves, Stattleman et al. (1975) compared the ab-
solute sensitivity thresholds of pigeons, bobwhite quail (Colin us vir-
ginianus) and domestic chickens to pentane, hexane, and heptane. These
workers found that all four species possess -10- 6 M sensitivity to these
odors, with pigeons being slightly more sensitive than the quail to
hexane and heptane but less sensitive than chickens to pentane and
hexane. In a comparison of olfactory sensitivity between pigeons and
the Black-billed Magpie (Pica pica), Snyder and Peterson (1979) de-
termined on the basis of changes in respiratory frequency that magpies
have absolute thresholds for butanethiol, ethanethiol, and menthol in
the range of 10- 3 _10- 6 M. Their findings also indicate that magpie
threshold sensitivities for ethanethiol and butanethiol are lower than
those for pigeons, while the reverse is true for menthol. Thresholds for
the detection of differences in odor concentration have also been mea-
sured in pigeons using standard laboratory chemicals such as cyclo-
hexane and are found to be on the order of 65% (Shumake et aI., 1969).
This value is approximately equivalent to that found in rats (Davis,
1973) but much poorer than human differential sensitivity, which can
be as good as 15-20% (Stone, 1963). Other experiments, however, have
failed to show an ability for pigeons to discriminate between environ-
mental air and filtered control air (Schmidt-Koenig and Phillips, 1978).
Only two direct tests of olfactory sensitivity to natural odors have
been attempted. Among the odorants tested by Snyder and Peterson
(1979) in their comparison of Black-billed Magpies and pigeons was
an extract of putrid meat, prepared by placing 50 g of ground beef in
20 ml of water and allowing the mixture to incubate for 2 weeks. Pigeons
showed no response to this odorant, whereas magpies did, suggesting
that a given odor may have species-specific olfactory relevance. Un-
fortunately, the way in which these stimuli were presented to the birds
does not permit a direct calculation of the concentrations of relevant
odorants involved. A more controlled test of sensitivity to biologically
meaningful odors comes from work on the Turkey Vulture (Cathartes
aura) by Smith and Pas elk (1986). Using heart-rate responses as an
indicator of sensitivity, they tested turkey vultures for absolute olfactory
thresholds to three by-products of animal decomposition: butanoic acid,
ethanethiol, and trimethylamine. Their results indicate that turkey vul-
tures can detect these odorants at concentrations as low as 1.0 x 10- 6 ,
1.0 X 10- 6 , and 10 x 10- 6 M, respectively.
Thus it appears that the lower limit of avian olfactory sensitivity
lies somewhere within the 10- 5_10-- 7 M range of odorant concentra-

tion. Whether biologically relevant odors are encountered in the bird's
environment at these or higher concentrations is in large part a product
of the physical properties of odor sources and the atmospheric con-
ditions that dictate the spread of odors in space and time.
4. CHEMICAL AND ATMOSPHERIC INFLUENCES ON

OLFACTORY ORIENTATION
Just like oceans, lakes, and rivers, the atmosphere is a fluid medium
that is constantly in motion. As a result, materials suspended in this
medium, including odors, are subject to the physical properties that
govern airflow in the atmosphere. This means that the movement of
airborne odors is strongly influenced by such parameters as temperature
gradients, pressure fields, and wind patterns, as well as by the surface
terrain features over which moving air passes. Moreover, the kinds of
natural odors available in the atmosphere are inextricably linked to the
ease with which odor molecules can be released from their sources (Le.,
their volatility). It is therefore essential to consider the interaction be-
tween the chemical characteristics of odor sources and the atmospheric
processes that influence both short- and long-range odor transport in
order to understand the ecological pressures that face birds when they
attempt to use odors as orientation cues.
4.1. Natural Sources of Odors

It should be clear from the preceding discussion that our under-
standing of what constitutes a biologically meaningful odor for birds,
and at what concentrations natural odors can be detected by the avian
olfactory system, is at best rudimentary. As such, a survey of possible
natural odor sources is of necessity reduced to an analysis of known
volatility and dispersion characteristics for substances that we can only
presume are potentially important odors for birds. These presumptive
olfactory stimuli obviously include the odors associated with food sources,
foliage smells, or other environmental odors associated with nests or
roosting areas, as well as the odors emitted by unique natural sources
that might be useful as landmarks or in the formation of olfactory nav-
igational maps.
Inorganic odors present in the atmosphere have two primary sources.
Some are anthropogenically derived and result almost exclusively from
mankind's burning of fossil fuels (Rice et a1., 1981). The other, and
globally more important, source of inorganic odors is naturally derived,

resulting from the release of odorant molecules at mineral deposits
that contain elevated levels of sulfur, ammonium, and other minerals
(Eriksson, 1963). These odor molecules become airborne primarily
through the creation of aerosols by wave action or evaporation from
bodies of water, as well as through vaporization processes from soils
(Dawson, 1977). To date, no natural inorganic odors have been used in
avian olfactory sensitivity experiments, and the question of whether
these chemicals fall within the realm of detectable or meaningful odors
for birds remains unanswered.
Many atmospheric odors, however, are biogenic in origin (Hitch-
cock, 1976; Adams et a1., 1981a,b). They can arise from a variety of
processes, including release of the enzymatic by-products of microbial
action in soil or water (e.g., ammonia, sulfur, or methane), the emission
of volatile secondary metabolites by plants (particularly the carotenoids
and terpenes), or the vaporization of odorants associated with certain
food sources (e.g., fish, carrion, ripening fruit, and flowers). Many of
these odors are common components of human foods and have there-
fore received considerable attention from chemists in the food-pro-
cessing and flavor industries (Parliment and Croteau, 1986). Their stud-
ies have concentrated, however, on the chemical properties and metabolic
pathways which produce organic odorants, and not on the occurrence
of these odorants in the atmosphere. As a result we have virtually no
direct data on normal emission rates nor ambient air concentrations
near the source of biogenic odors.
Nevertheless, it is clear that these odors do get into the atmosphere
at levels detectable by animals, as witnessed by observations of olfac-
tory prowess in many macrosmatic vertebrates, especially the terrestrial
mammals, which regularly use natural odors as behavioral cues (Stod-
dart, 1980). Even our own memory-evoking experiences with natural
smells serve to indicate that the atmosphere contains a complex set of
olfactory cues for those organisms capable of detecting it (Engen, 1987).
In a sense, humans are not unlike birds, in that we are both technically
considered microsmatic vertebrates. Yet we are aware from personal
experience of the many environmental subtleties that can be detected
using the sense of smell. It seems reasonable to consider that, while
they may not be equivalent to most mammals in terms of olfactory
prowess, birds may still be capable of extracting useful olfactory in-
formation from the environment.
Important in determining whether airborne olfactory stimuli exist
at sufficiently high ambient concentrations to permit detection by birds
is an understanding of emission rates for odorant sources, but few
OLF ACTORY ORIENT ATlON 279
specific data exist. Although large quantities of inorganic and organic

odorants are released worldwide on an annual basis, e.g., the yearly
sulfur output from natural sources located between 30° and 50° N alone
is estimated at 1.7 x 10 7 metric tons (Eriksson, 1963), measurements
of specific emission rates for localized geographical areas are rare. The
few that exist estimate sulfur and ammonia emissions as being <10
kg/ha per day, which results in ambient atmospheric concentrations
near the source of ~10 - 9 M (Graedel, 1978). Estimates of emission rates
for plant terpenes (e.g., a-pinene) emanating from the pine-oak forests
of the United States yield daily values of about 1-5 kg/km2 of woods
(Rasmussen, 1972). This rate of emission produces ambient air con-
centrations directly above the wooded area of 10 - 7 M.
The natural concentrations of volatile alcohols and carbonyls re-
sponsible for the aroma of freshly caught fish have also been measured
Uosephson and Lindsay, 1986). These chemicals are present at 10- 7-10- 10
M concentrations in the skin secretions of a wide variety of fish species,
and their synthesis is apparently stress related (Fletcher, 1981). Thus,
we presume that fish odors would commonly be present in the air above
areas where man or other animals are actively harvesting fish, or where
one species of fish is interacting with another species near the water's
surface. While no direct measurements of ambient air concentrations
have been made in these areas, it seems highly likely that concentrations
of at least 10 - 9 M if not higher are present for detection by birds flying
in the vicinity of these aromas (R. C. Lindsay, personal communication).
If these few estimates of ambient air concentration for natural odors
are representative of other orientationally meaningful odors in the at-
mosphere, our current understanding of avian olfactory sensitivity
thresholds (i.e., absolute sensitivities of 10 - 5-10 -- 7 M) permits the con-
clusion that birds are just able to detect at least some odor cues from
the environment. It is important to emphasize, however, that the exact
concentrations and daily emission rates of biogenic chemical sub-
stances are not well-established empirically, especially considering that
they are often subject to daily and seasonal fluctuations which could
significantly affect ambient concentrations by several orders of mag-
nitude. Thus, emission rates and concentration values are to be taken
as approximations only. It is therefore unclear whether most natural
sources of potential avian olfactory cues emit odorants at rates that
create physiologically reasonable concentrations more than a few tens
or hundreds of meters from their source, at least not without the aid
of some atmospheric factor that helps concentrate the odor. However,
if we operate on the assumption that at least some odor sources do emit
odorants at levels sufficient to generate physiologically reasonable con-
centrations in the atmosphere, the next step in our analysis is to de-

termine the fate of these odors, both spatially and temporally.
4.2. Mechanisms of Odor Dispersion

As odor molecules disperse from their source, odor concentrations
in the air decline with increasing distance. In still air at very short
distances (Le., a few meters or less), this dispersion is governed pri-
marily by the laws of molecular diffusion. In nature, however, still air
is the exception rather than the rule; thus, simple diffusion is replaced
by longer-range transport in a moving air mass. As a result, most odors
end up being carried downwind from their source, where they tend to
be dispersed by turbulence and other atmospheric processes. Put an-
other way, at one end of the spectrum of atmospheric odor dispersion,
simple diffusion dictates the ambient concentration of odor molecules,
while at the other end, dispersion patterns are governed by larger scale
processes, such as convection, advection, wind shear, and turbulence.
Given that olfactorially guided bird behaviors have the potential to
range from localized foraging up to long-distance migration and navi-
gation, a brief examination of the mechanisms responsible for both
extremes of atmospheric odor dispersion is in order.
Short-range atmospheric odor transport has been successfully stud-
ied using simple diffusion and Gaussian plume models, particularly
with respect to its influences on the use of pheromones by insects
(reviewed by Elkinton and Carde, 1984). An important concept at this
level of analysis involves the so-called active space of an odor, defined
as the volume of air inside which the odor concentration is above
threshold, i.e., the level sufficient to produce a behavioral reaction in
an organism capable of detecting the odor. The dimensions of an active
space in still air can be defined using simple principles of diffusion,
resulting in the following equation for a continuously emitting source:
Rmax = Q/2K 7TD
where Rmax is the maximum radius of the active space, Q is the amount
of odorant released (in grams), K is the behavioral threshold, and D is
the diffusion coefficient (Wilson et a}" 1969). This equation provides
a simple way for estimating the maximum limits of an active space
based on the diffusion characteristics of odors in a still air environment.
Theoretically, it can thus be used to determine the maximum distance
over which a bird might detect short-range odor cues that are useful in
locating a concealed food source or nest. Figure 1a shows the hemi-
a Sill! Air
FIGURE 1. Short-range patterns of odor dis-

persion in the atmosphere. Solid spot indi-
cates an odor source, and stippled region
represents the surface area covered by the b Movipg Air - - +
volume of active space above it. (a) Hemi-
spherical active space with radius Rmax that
forms in still air. (b) Active space that forms
in moving air, with its odor plume oriented
downwind of the source. Xmax is the maxi-
mum distance from the source at which the
odorant can be detected.
spheric shape that this active space will assume, given a continuously
emitting source located on a flat nonabsorbing surface.
Our working knowledge of the chemical nature of relevant avian
olfactory stimuli, combined with a minimal understanding of the limits
of avian odor sensitivity, render the above equation impossible to solve
accurately because of the existence of more than one unknown variable;
i.e., Q, K, and D are not known for birds or the odors they can detect.
However, if we examine the case of insect pheromone signaling, where
Q/K ratios have been empirically determined to range between 10 2 and
10 12 molecules/cm 3 and where diffusion coefficients for pheromones
vary between 0.03 and 0.07 cmz/sec, we find that Rmax for this form of
chemical detection is on the order of tens to hundreds of centimeters'
(Bossert and Wilson, 1963). By analogy, if we assume that Q/K ratios
for birds are on the lower end of those values measured for insects (e.g.,
10 2 -10 4 ). and also that the volatility of odor molecules of interest to
birds does not exceed that of insect pheromones, an estimate of Rmax
for birds results in an active space not larger than a few meters in
diameter. An active space of this size might be useful in locating the
source of nearby food but would clearly be of no value in longer-range
orientation.
In the more likely condition of moving air, an odor plume is created
downwind of the odorant source (Fig. 1b). The dimensions and shape
of this plume depend on several factors, including not only the ground
surface characteristics and the emission rate of the odorant, but also
the mean wind speed (Sutton, 1947, 1953). The odor concentration
along any axis perpendicular to the downwind direction of the plume
is assumed to follow a normal or Gaussian distribution. Wright (1958)
and Bossert and Wilson (1963) independently introduced the use of
the Gaussian dispersion equations to the analysis of insect pheromone

dispersion in wind and solved the equations for the maximum distance
of chemical communication:
where Xmax is the maximum distance, Q and K are defined as in the

previous equation for still air dispersion, Cy and Cz are the horizontal
and vertical concentrations, respectively, n is an index of the vertical
wind-speed profile, which varies between 0 and 1, and u is the mean
advecting wind speed (i.e., the horizontal wind responsible for down-
wind movement). In insects such as the gypsy moth (Lymantria dispar),
which have evolved an extremely sensitive, species-specific pheromone
signaling system with a QIK ratio in excess of 10 10 , analysis using
Gaussian dispersion models shows that chemical communication is
possible over a distance of 4 km, under ideal conditions (Bossert and
Wilson, 1963).
Diffusion coefficients for naturally occurring ambient odors have
not been measured, nor have QIK ratios been determined for birds.
However, it is virtually certain that the volatility of most ambient odor-
ants does not match that of insect pheromones, since the compounds
that make up pheromones have often been intensely selected for high
volatility characteristics to enhance dispersion, whereas ambient odors
have not. Moreover, the threshold for a behavioral response K in the
pheromone-driven orientation of insects is very likely lower by orders
. of magnitude than that of birds, as indicated by each group's absolute
olfactory thresholds. For example, while birds have olfactory thresholds
on the order of 10- 6 M (Stoddart, 1980; Bang and Wenzel, 1985), many
insects are sensitive to pheromones at concentrations of 10- 15 M (Elk-
inton and Carde, 1984). Conversely, the number of odorant molecules
released from the source and available in the atmosphere for detection
Q is certainly higher for ambient odors than for pheromone molecules,
which are often released in microgram quantities. Arbitrarily assigning
a value of 10 7 for the QIK ratio of birds, and given the identical wind
conditions used to calculate the 4-km maximum pheromone-signaling
distance for the gypsy moth, we thus obtain an estimate of Xmax that is
several orders of magnitude less than this 4-km distance, reducing the
effective range over which birds can detect an odor to a few tens or at
most hundreds of meters. Regardless of whether the actual QIK and
Xmax values for birds turn out to be lower or higher than this estimate,
the use of such Gaussian plume models clearly demonstrates that ol-
factory plumes of reasonable dimensions are possible under appropriate
OLFACTORY ORIENT A TION 283
atmospheric conditions. Therefore, once a bird that is behaviorally sen-

sitive to an odor comes in contact with the appropriate plume, simple
anemotaxic (upwind) orientation could allow for location of the odor
source.
Larger-scale processes of atmospheric dispersion, such as the long-
range transport of pollutants, have been successfully analyzed using
synoptic (large )-scale mathematical-physical models that relate rates
of emission to prevailing meterological conditions (reviewed by Elias-
sen, 1980). When considering long-range dispersion of particles or odors
in the atmosphere, it is often convenient to think in terms of a com-
bination of advection and turbulent diffusion (Gttar et a1., 1984). As a
plume of odors is advected, simultaneously turbulence consisting of
eddies of many different sizes disperses the odors in both vertical and
lateral directions, so that the size of the plume is increased in time and
space. Vertical and lateral diffusion of the plume depends strongly on
the atmospheric conditions present in the so-called boundary or mixing
layer, the lowest few thousand meters of the atmosphere, where most
synoptic activity occurs. Under normal conditions, the influence of
turbulent diffusion is most important during the first few kilometers of
transport downwind from the source (Pasquill, 1974). After traveling
this distance, the vertical distribution of odors or particulate matter is
more or less uniform within the mixing layer. When mixing is complete
in the vertical, it appears that one may, at least to a first approximation,
assume that the air mass carrying the odor is directed solely by advec-
tion. Thus, surface-level trajectories of air parcels (Fig. 2) can provide
reasonable predictors of long-range odor transport patterns (Ferber et
aI., 1986; Waldvogel, 1987).
Such one-layer models are not always realistic, however. Under
very stable conditions, when turbulence is greatly reduced, for example,
plumes may travel long distances with relatively little odor dilution.
Thus, the extent of long-range transport and its overall effects on odor
concentration within the plume strongly depend on the details of cur-
rent synoptic meteorological conditions. The height of the mixing layer
within which odors are assumed to be well mixed is also an important
factor. For example, inversions at heights of a few hundred meters will
create an upper limit beyond which no mixing can occur. But often no
such limit exists. Moreover, natural mixing heights undergo diurnal
variations, being low during the night and highest in the early afternoon
(Smith and Hunt, 1978). Diurnal variations of mixing heights with the
concomitant buildup of a stable ground inversion during the night often
prevent elevated plumes from reaching the ground. When the inversion
breaks up the following day, convective (vertical) mixing occurs, driv-
I .5
[
d
FIGURE 2. Examples of surface trajectories for air parcels labeled with a tracer gas and subsequently tracked by 100 ground-sampling stations
located across the northeastern United States. In each of the four cases shown (a-d), 180-210 kg of gas was released over a 3-hr period from Dayton,
Ohio (R) in the autumn of 1983. Trajectories were visualized by plotting lines of equal concentration , measured in femtoliters/liter (10 - 1 5 M) . Each
plume represents the maximum concentration of tracer observed during the 50-hr postrelease period. (From Waldvogel, 1987; after Ferber et aI. ,
1986.)
ing the odor downward to the surface and creating problems of direc-
tional ambiguity for a bird that is trying to extract orientational infor-
mation from the odor cue. At latitudes in excess of 40°, large-scale
inversions of this type may have profound effects on the long-range
transport of particulate matter and odors in the atmosphere (Eliassen,
1980; Ferber et al., 1986).
Measurements of the vertical distribution of substances such as
sulfur dioxide and sulfate particles in Europe have shown that pollu-
tants are in general contained within the lowest 2000 m of the atmos-
phere, with maximum concentrations at a few hundred meters above
the ground (Gotaas, 1980). Both wind speed and wind direction change
substantially with height within this layer, complicating the prediction
of particulate or odor transport due to the difficulty of defining a single
advecting wind. This not only has implications for modelers of atmo-
spheric processes but also creates problems of directional ambiguity
for birds that choose to use odor information that has been sampled
aloft, especially at different altitudes over approximately the same geo-
graphical location. Becker and van Raden (1986) analyzed airflow pat-
terns in the vicinity of a German power plant and determined that
surface level winds do not exhibit sufficient regularity to act as reliable
carriers of directional odor information and are therefore not likely to
be effective in providing useful olfactory landmarks or maps. Waldvogel
(1987) found similar drawbacks to the possibility of olfactory navigation
by pigeons flown in the northeastern United States, based on observed
surface-level trajectories of plumes that had been marked by a tracer
gas and then tracked in the pollution transport studies of Ferber et al.
(1986). These studies also demonstrate the dramatic dilution of odors
which occurs over distance. The presence of a harmless tracer gas (per-
fluoromonomethyl cyclohexane: C7F14), which was released from source
points in Ohio and Ontario at rates of 60-70 kg/hr over a 3-hr period,
was subsequently detected just 200-300 km downwind of the source
in concentrations of only 10- 12 M (Fig. 2).
Another feature of atmospheric influence on airborne olfactory cues
involves the effects of terrain features. These physical obstacles to air-
flow are common features of many geographical areas and can also be
responsible for indirect changes of airflow caused by the effects of
differential heating over irregular surfaces. Included among these at-
mospheric phenomena are the downslope winds and obstruction cur-
rents commonly observed along mountain ranges, thermals that develop
over ridge tops, and sea breezes frequently encountered along extended
shorelines. All these phenomena cause significant redirection or chan-
neling of either horizontal or vertical winds and thus the odors carried
on those winds. This modification of "normal" windflow can either act

to enhance, disrupt, or provide erroneous directional olfactory infor-
mation, depending on whether convergence or divergence of airflow is
the end result. Indeed, a good possibility exists that some of the ap-
parent geographical specificity observed in olfactory orientation ex-
periments performed with homing pigeons in different countries may
results from the influence of terrain-modified patterns of windflow (Papi,
1986; Schmidt-Koenig, 1987; Waldvogel, 1987; see also Section 5).
In summary, where and when a bird will encounter a given con-
centration of some relevant ambient odor is dictated almost exclusively
by physical properties of atmospheric dispersion and long-range trans-
port. In instances in which the objective is to track an odor to its source,
as is the case in foraging, the distance over which this objective can
realistically be attained depends on the emission rate of odorant mol-
ecules, the extent of odor dilution in the atmosphere due to turbulence
and mixing, and the behavioral threshold of the bird for the odor(s) in
question. In cases in which odors may be used to establish landmarks
or construct a navigational map, the distances over which they can be
effective depends in large measure on the degree of stability exhibited
by the transport mechanisms that disperse the odors. The significant
influence that atmospheric processes have on odor dispersion is there-
fore a crucial element to be considered in the behavioral analysis of
avian olfactory orientation.
5. BEHAVIORAL EVIDENCE FOR THE USE OF ODORS IN

AVIAN ORIENT A TION
While careful physiological analysis of olfactory sensitivity and

the precise measurement of atmospheric odor concentrations are es-
sential to a thorough analysis of olfactory orientation, neither is as
persuasive as data from rigorous behavioral demonstrations of odor
usage by birds. During the past 15 years, there has been a dramatic
increase in the number of field tests that claim to show olfactory influ-
ences on orientation behavior in birds. The remainder of this chapter
is devoted to a discussion of these behavioral data, which have been
organized according to my impression of how best they reflect the three
types of orientation presented in Section 2.
5.1. Odors as Landmarks

There is no doubt that olfactory landmarks provide a major source
of directional information for many organisms. Virtually every animal
phylum with members that are capable of movement has representa-

tives for which some level of olfactory orientation has been demon-
strated. Vertebrates in particular have been well studied for their ability
to orient with respect to olfactory landmarks (Stoddart, 1980). Familiar
to everyone are such spectacular examples as the olfactory homing
ability of adult salmon, the sophisticated chemical pursuit behavior
employed by many species of poisonous snakes to track invenomated
prey, or the precise olfactory trailing ability exhibited by canids. Until
recently, however, examples of birds that derive useful directional in-
formation from odor landmarks have been conspicuously absent from
discussions of vertebrate olfactory prowess. This situation is changing,
however, as more and more evidence accrues in favor of a functional
sense of smell in birds. In the cases of olfactory landmark orientation
by birds that have so far been reported, orientation has either involved
localization of an odorus food source or nesting burrow, or the use of
odor cues to choose among possible foods or nesting materials. Several
of these cases of olfactory orientation appear to be best analysed using
the concept of a short-range active space, while others come under the
heading of longer range orientation using an olfactory plume estab-
lished downwind of the source.
5.1.1. Short-Range Responses to Olfactory Landmarks

Conditions of still air permit the development of a stationary ol-
factory active space that might be of use to birds in such behaviors as
pheromone signaling or searching for nearby concealed food items (see
Section 4.2). To date there has been little more than speculation con-
cerning the possibility that pheromones might playa role in avian
behavior, in part due to an apparent lack in birds of highly specialized
secretory glands like those commonly found in mammals (Wenzel, 1985).
Birds do, however, possess a variety of secretory glands that may serve
as sources of olfactory signals. The most obvious is the uropygial gland,
which is present in all but a very few species. While the role of this
gland has traditionally been viewed as providing lipid secretions used
to confer water repellancy on feathers, it is also known for some species
that the weight of this gland and its chemical composition change
markedly during the breeding season. In the European rook (Corvus
frugilegus), the uropygial gland doubles in weight during courtship and
nesting compared with other phases of the breeding cycle (Kennedy,
1971). Female mallard ducks (Anas platyrhynchos) exhibit seasonal
fluctuations in the chemical composition of uropygial gland secretions,
showing significant differences between the breeding season and other
times of the year (Jacob et a1., 1979). Behavioral evidence that this
change in chemical composition may mediate important aspects of
courtship and breeding behavior comes from experiments by Balthazart
and Schoffeniels (1979) in which significant inhibition of sexual be-
havior was observed in male mallards that had been subjected to bi-
lateral sectioning of the olfactory nerve. Other behaviors that were mon-
itored appeared to be unaltered by the surgical intervention. Such data
imply that secretions from the female mallard's uropygial gland can
act as stimulants for normal sexual behavior in males.
External and internal anal glands are also present in birds, as well
as cloacal glands (Quay, 1967). No chemical studies of these glands
have been conducted, and their function remains obscure. Sebaceous
secretory tissue such as the Harderian gland exists in the orbit of the
eye, and other such tissue is located in the external ear. Specialized
glandular cells which secrete sebaceous materials can also be identified
throughout the skin, but the function of these cells so far is unknown.
Many species, especially pelagic seabirds, produce a highly odo-
rous stomach oil which may have specialized olfactory signaling power.
Wenzel (1985) discusses the possibility that the chemical composition
of stomach oils produced by the procellariids may be under sufficient
genetic control to permit individual recognition on the basis of odors.
Since stomach oil is frequently emitted by nestlings and adults as part
of a defense mechanism aimed at diverting the attention of predators,
the area around the nesting burrow of procellariids is usually marked
by considerable quantities of this odorous substance. Several sugges-
tions (reviewed below) have been made that this odor cue provides a
necessary and sufficient olfactory landmark to permit adults to identify
the home colony and their own nesting burrow upon returning from
nocturnal foraging trips at sea. Reports of increased heart rate in re-
sponse to mate or burrow odors made by Grubb (1974) for Leach's
Storm-petrels (Oceanodroma 1eucorrhoa) and by Shallenberger (1975)
for Wedge-tailed Shearwaters (Puffinus pacificus) tend to support these
suggestions, although additional psychophysical research with strict
physiological controls must be performed to verify these findings.
Another use for short-range olfactory cues is in foraging. The brown
kiwi (Apteryx australis) has received particular attention in this regard
because of its peculiar olfactory anatomy and distinctive foraging habits
(Benham, 1906). Kiwis are nocturnal and, unlike many other night
active birds, possess relatively poor eyesight. Much of their active pe-
riod is spent searching in the damp soil of heavily forested areas for a
staple diet of earthworms and insect larvae. While foraging an audible
sniffing sound is produced as the bird probes the earth with its long
beak, at the distal tip of which are located the nares. Indeed, the three
living species of kiwis are the only extant birds with such a placement
of the nares. Convincing evidence for a functional sense of smell that
forms the basis of kiwi foraging was collected by Wenzel (1968, 1971)
in experiments in which baited aluminum feeding tubes were filled
with an odorous mixture of raw meat, raisins, and poultry starter mash
and then buried below the ground's surface. Besides being covered with
a 3-cm-deep layer of dirt to prevent visual inspection of the feeding
tube's contents, each tube was also covered with nylon screening, which
the bird had to puncture in order to reach food, thereby leaving a
permanent record of whether a tube had been investigated. In tests
using captive kiwis housed in a seminatural enclosure, each bird was
given the opportunity to choose between baited tubes and otherwise
identical control tubes filled with moistened soil only. In all cases, they
invariably selected the baited tubes and ignored the unbaited ones.
Wenzel also recorded reliable respiratory and electroencephalographic
(EEG) responses to the odors associated with food, in addition to suc-
ceeding in demonstrating conditioned aversive responses to foods scented
with the mildly noxious chemicals amyl acetate, trimethylpentane, pyr-
idine, and synthetic musk. These results demonstrate that kiwis are
indeed macrosmats, and that their highly developed sense of smell
provides the primary sensory input used in foraging.
Additional evidence for the use of odors to find hidden food comes
from a study of the Black-billed Magpie (Buitron and Nuechterlein,
1985). Magpies, as is the case for most corvids, engage in caching be-
havior. In field experiments designed to determine the nature of the
cues used to relocate these caches, Buitron and Nuechterlein found that
Black-billed Magpies uncovered significantly more caches of suet and
raisins scented with cod liver oil than of unscented control caches.
These investigators suggest that while magpies probably use a multi cue
system involving both memory and visual or olfactory cues to recover
caches, olfaction may be particularly important in finding and taking
food that has been hidden by other individuals. Anecdotally, these
workers also report an instance in which magpies discovered a com-
pletely hidden chicken that had begun to smell after being placed be-
neath a submerged rock in a small stream. This meat had been "cached"
by humans 1 week previously while still fresh and was discovered by
the magpies only after it had begun to decay. Such reports are consistent
with laboratory studies of olfaction (see Section 3), in which magpies
show a clear-cut olfactory response when presented with the odor of
putrid meat extract (Snyder and Peterson, 1979).
Goldsmith and Goldsmith (1982) succeeded in both positively and
negatively conditioning Black-chinned Hummingbirds (Archilochus 01-

exandri) to artificial feeders baited with either a 30% solution of sucrose
(attractive stimulus) or a 3% saline solution (aversive stimulus). The
odorant used was ethyl butyrate, the odor of which is reminiscent of
Juicy Fruit chewing gum. In the absence of visual cues, the birds quickly
learned to differentiate between the sucrose and saline solutions, dem-
onstrating not only that Black-chinned Hummingbirds have a func-
tional sense of smell, but also raising the possibility that this sense may
be used in conjunction with their well-developed vision in order to
discriminate between the cues presented by different species of flow-
ering plants competing for the attention of bird pollinators.
Two other cases involving the use of short-range odor cues in avian
foraging have been reported. Jarvi and Wiklund (1984) studied food-
choice preferences in Great Tits (Porus major) after the maggots (Cal-
liphora sp.) on which the birds were feeding had been tainted with
either bitter almond oil or maize oil. The tits quickly learned to dis-
criminate between the distasteful and palatable insect larvae, although
neither group of maggots' behavior or color (i.e., visual cues) differed
after treatment with the oils. In a test of olfactory influences on feeding
behavior in juvenile geese (Anser a. anser and Anser domesticus), Wur-
dinger (1979) found that goslings start reacting to odors at 11-20 hr
posthatching, showing head-shaking behavior to the odors of plants on
which adult geese refuse to feed (e.g., lavender and violet). By age 4-9
days, goslings show quantitatively different reactions to different odors
such as sage, dwarf pine, and dill. In addition, goslings quickly become
habituated to odors and will no longer react if an odorant is presented
repeatedly.
Finally, recent reports by Clark and Mason (1985, 1987) suggest
that birds may also use short-range olfactory cues to select among pos-
sible nesting materials on the basis of their utility as insecticidal or
anti pathogenic agents. Multiunit electrophysiological recordings from
the olfactory nerves of European Starlings (Sturnus vulgaris) show that
reliable olfactory responses are evoked upon presentation of volatile
extracts from several of the plant species commonly found in starling
nests. Moreover, after pairings of these plant volatiles with gastroin-
testinal malaise, the birds exhibit conditioned avoidance in subsequent
behavioral experiments and are able to make all possible pairwise dis-
criminations successfully among the various volatile substances.
A variety of evidence thus exists for the use of short-range odor
cues by birds. One extremely important aspect of these studies is the
indication of behavioral sensitivity to olfactory stimuli not only in birds
with large ratios of olfactory bulb size to brain hemispheric dimensions
(e.g., birds with ratios >25% such as kiwis and procellariids), but also
in species with very small ratios (e.g., tits and starlings, whose ratios
are <15%). The small size of olfactory neural tissue should therefore
no longer be taken as sufficient evidence against the likelihood of good
odor discrimination by birds, nor as evidence against the feasibility of
at least simple forms of avian olfactory orientation.
5.1.2. Downwind Responses to Olfactory Landmarks

Odor detection at distances greater than a few meters from the
source is also documented in several avian groups. The best known
example is the foraging behavior of new world vultures. Early settlers
of the Americas were quick to note the impressive ability of vultures
to congregate at the site of a decaying animal, even if no visual cues
were available (Audubon, 1826). The birds were thus granted in folklore
an image of powerful olfactory prowess. Modern experiments dem-
onstrate that Turkey Vultures do in fact possess a large olfactory system
as well as a highly functional sense of smell (Owre and Northington,
1961; Stager, 1964; Smith and Paselk, 1986) and, by using carrion odors,
they are thus able to forage effectively. The Black Vulture (Coragyps
atratus), which is sympatric with the Turkey Vulture over many parts
of its range, appears to be primarily a visually guided scavenger, a
finding that is perhaps in keeping with the relatively small size of its
olfactory bulbs (Stager, 1967). Conflicting reports exist, however, as to
whether other New World vultures also use olfactory orientation while
foraging. Stager (1964) indicates that the King Vulture (Sarcorhamphus
papa) probably possesses a good sense of smell based on an analysis
of olfactory anatomy, but Houston (1984) disagrees on the basis of
controlled feeding tests with three captive birds that showed no evi-
dence of using odors to detect hidden food. Rather than being olfac-
tori ally guided foragers, Houston suggests that King Vultures are pri-
marily visual scavengers that take advantage of the ability of the sympatric
Turkey Vulture to locate carrion by olfaction and then displace the
smaller Turkey Vulture once a food source has been found.
Another group of birds in which olfactory orientation is observed
is the family Indicatoridae, the honeyguides. These small sparrow-sized
relatives of the woodpeckers and toucans subsist in part on the wax
used by honeybees to construct their comb (Friedmann and Kern, 1956).
Stager (1967) conducted a simple test in Africa in which he put a single
beeswax candle in the crotch of a tree and observed that, as long as the
candle was unlit, no honeyguides could be seen in the area. Shortly
after lighting the candle, however, honeyguides appeared and began to
OLF ACTORY ORIENTA nON 293
feed on the melting wax. Under natural conditions, honeyguides lead

large mammals such as honey badgers (Mellivora capensis), baboons
(Papio sp.), or man to beehives and then feed on the larvae and wax
that remain after the hive has been raided (Archer and Glen, 1969).
Beehives normally produce a pungent odor, and it is assumed (although
not proved) that it is this smell that attracts the birds either to a natural
hive or to the smoke of a burning beeswax candle. Gross anatomical
analysis of the skulls of several species of honeyguides shows a well-
developed olfactory bulb and epithelium (Stager, 1967), although no
precise measurement of olfactory ratio or physiological response to
odors has yet been made for any member of this family.
Large olfactory structures also characterize the oilbird (Steatornis
caripensis), a large relative of the night jars from equatorial Latin Amer-
ica. Oilbirds forage on the wing, feeding on the aromatic and spicy fruit
of local palm trees (Snow, 1961). Since not all trees produce ripe fruit
simultaneously, odor cues may provide the sensory basis for selecting
between ripe edible fruits and green unpalatable ones (Stager, 1967).
This species therefore represents an excellent candidate for controlled
tests of olfactory sensitivity to natural odors, since the presumed source
of olfactory cues (Le., the fruits on which the bird feeds) is known. To
date no such tests have been reported.
The odor plumes that form in moving air are predominantly ori-
ented downwind from their source and can often rise to relatively high
altitudes (see Section 4.2). In the case of vultures, honeyguides, and
oilbirds, food sources are probably localized as a result of olfactory
plumes that form in both vertical and horizontal dimensions. The extent
to which vertical mixing occurs in an otherwise horizontally propa-
gating odor plume will depend in large measure on the nature of the
terrain over which the plume passes. On land, where air warmed near
the surface tends to rise very rapidly, vertical movement of odor mol-
ecules within a plume can be substantial (Lutgens and Tarbuck, 1982).
Over water, by contrast, where surface heating is much less dramatic
compared with land, vertical motion is reduced and odors tend to
remain closer to the surface. This tendency for well-defined low-level
odor plumes to form over water may have been a driving force behind
the development of olfactory foraging in several species of procellariids,
birds for which an increasing body of anatomical and behavioral data
suggests a highly developed sense of smell.
Sailors have long known of the tendency for shearwaters, fulmars,
and petrels to congregate downwind of ships when warm animal fat
or offal is scattered on the water (Murphy, 1936; Miller, 1941). Casual
observations reported by Stager (1967) suggest that these birds can
easily distinguish between animal fat and other oils such as those used
in the manufacture of paints. These fats and oils also emit a musky
odor that can be detected by humans from many miles downwind of
a breeding colony. Procellariiform birds have well-developed olfactory
neural tissue and large convoluted nasal cavities supporting extensive
olfactory mucosa (Bang and Wenzel, 1985). Most species live and breed
in temperate to subpolar climates and maintain a highly pelagic life-
style. Their tendency to forage many miles out to sea, where reliable
visual cues are uncommon, places demands on other sensory channels
to provide long-range detection capabilities. Wenzel (1985) speculates
that the very large olfactory system of procellariids might be an ad-
aptation to a life-style that finds them breeding and foraging in ex-
tremely cold climates where the volatility of food- and nest-related
olfactory cues is low, but where no other sensory modality can provide
the necessary long-range detection sensitivity to find food sources and
nesting burrows from comparable distances.
Grubb (1974) monitored nocturnal arrivals with respect to wind
direction at the nesting colony of Leach's Storm Petrel. He found that
birds returning to the colony at night did so primarily from the down-
wind direction, hovering above the spruce-fir canopy momentarily
before dropping to the forest floor. It is not clear, however, whether this
behavior is more a result of olfactory orientation or of an aerodynamic
aid to the unus·ual landing requirements dictated by the heavy foliage
covering this particular colony. After landing, the birds tended to walk
upwind towards their burrows. On nights with still air, the birds fol-
lowed a more circuitous route to the nest. Petrels transported from the
colony after having their nares plugged with modeling clay or their
olfactory nerves transected did not return within 1 week's time, whereas
sham-operated and untreated birds did. However, James (1986) could
not find similar evidence for olfactory orientation in his study of Manx
Shearwaters (Puffinus puffinus) at a breeding colony in the United
Kingdom. He concluded that visual cues are more likely the orientation
signal used for burrow location in this species. Likewise, Shallenberger
(1973, 1975) determined that vision probably also provides the domi-
nant orientation cue for Wedge-tailed Shearwaters returning to a nesting
colony in Hawaii.
Experiments designed to explore the possibility that olfaction func-
tions as an aid in procellariid foraging, rather than as an orientation
cue for finding the nesting colony, seem to have produced more inter-
nally consistent results. Jouventin (1977) demonstrated that the Snow
Petrel (Pagodroma nivea) can find scraps of raw fish concealed in plastic
cups or buried in the snow, whereas the South Polar Skua (Stercorarius
• Cod liver oil D Seawater
'"
= 100
=
E
....
....'"o 75
E
...-= 50
I:
~
.;
:c'"
101)
25
c
~ 0
Wilson's Leach's Snow Cape Greater
storm storm petrel petrel shearwater
petrel petrel (8) (8) (b)
<a,b) (b)
FIGURE 3. Investigative behavior exhibited by five species of procellariiform birds flying

in the vicinity of odorous and nonodorous stimuli. Data are plotted as the percentage of
investigative flights that came within 10 m of a floating sponge soaked in either cod liver
oil or seawater. Values in parentheses indicate the number of flights on which the per-
centages are based. a, Antarctic data from Jouventin and Robin (1984); b, Canadian
maritimes data from Grubb (1972).
maccormicki) cannot. In night tests conducted in the Bay of Fundy

using free-floating sponges soaked in either cod liver oil or seawater,
Grubb (1972) obtained convincing evidence that Leach's Storm Petrel,
Wilson's Storm Petrel (Oceanites oceanicus), and Greater Shearwaters
(Puffinus gravis) make significantly more approaches from the down-
wind direction to an oil-soaked sp'Jnge than to the control stimulus.
Similar results were obtained by Jouventin and Robin (1984), who showed
in their study of Antarctic procellariiforms that Wilson's Storm Petrels,
Snow Petrels, and Cape Petrels (Daption capense) all exhibit a signif-
icant increase in investigative behavior toward a sponge scented with
cod liver oil compared with a seawater control. The results of these
two studies are summarized in Fig. 3. Working in the Eastern Pacific
Ocean off California, Hutchison and Wenzel (1980) and Hutchison et
a1 (1984) demonstrated significant downwind attraction to floating ol-
factory stimuli for several additional species of procellariids, including
TABLE II
Percentage Downwind Approaches to Food-Related Olfactory Stimuli by
Three Species of Seabirds. a-c
Whole cod liver oil Cod liver oil fraction
Species N 50 m 10 m N 50 m 10 m
Sooty shearwater 60 60 50 43 80 70
(Puffinus griseus)
Northern fulmar 23 80 50 7 100 100
(Fulmarus glacialis)
Western gull 124 30 10 60 20 0
(Larus occidentalis)
"Data from Hutchison et 01 .. 1984.

bTwo stimuli. whole cod liver oil and the volatile fraction of cod liver oil. were independently released
at sea from floating wicks.
'Data for two approach distances (50 m and 10 m) are shown; N = number of flights observed.
dPercentage downwind defined as approach toward the olfactory stimulus from within the area
encompassing 45° on either side of the mean downwind direction.
Sooty Shearwaters (Puffinus griseus), Northern Fulmars (Fulmarus gla-

cialis), Pink-footed Shearwaters (P. creatopus), Black-footed Alba-
trosses (Diomedea nigripes), and Ashy Storm Petrels (Oceanodroma
homochroa). Whole cod liver oil and an extract of the volatile fraction
from cod liver oil were among the odors used as attractants. Table II
shows the large percentage of downwind approaches observed for two
of the procellariids studied. Also shown are approach data for Western
Gulls (Larus occidentalis), which failed to exhibit any directional ten-
dency when approaching an odor stimulus. Visual foraging cues such
as pieces of puffed cereal scattered on the water's surface were, how-
ever, highly effective in attracting such nonprocellariid species as gulls
(Hutchison et al., 1984).
Finally, an interesting observation concerning the mechanism by
which procellariids localize an odor source has emerged from the work
of Hutchison and Wenzel (1980). After coming in contact with the odor
plume somewhere downwind of the source, they report that the bird
initiates a search for the source of this odor by turning upwind and
executing a zig-zag flight pattern in and out of the odor plume (Fig. 4).
This search pattern is highly reminiscent of the zig-zag flight exhibited
by male moths during upwind anemotaxis toward a sexually receptive
pheromone-emitting female (Kennedy and Marsh, 1974). Such a path
is the most efficient way of maintaining position within an olfactory
plume while working up an odor gradient toward the source.
It thus appears virtually certain that some bird species are capable
WIND
FIGURE 4. Diagrammatic representation of the

flight response (solid line) of a procellariiform
bird after it has encountered a food-related odor
plume (shaded area) while foraging at sea. Sur-
face level winds (arrow) dictate the downwind
movement of this olfactory active space. The
zig-zag upwind flight pictured here represents
the most efficient strategy for localizing an odor
source in moving air and is reminiscent of the
flight pattern observed for insects responding to
airborne pheromone cues. (After Hutchison and
Wenzel, 1980.)
of detecting and localizing the source of meaningful odors in order to

gather nesting materials, locate a nest site, or forage. This ability seems
to operate over ranges of a few meters for some species (e.g., kiwis,
magpies, geese, tits, and starlings), while other species (e.g., vultures,
honeyguides, oilbirds, and procellariids) take advantage of odor cues
over much longer distances, possibly extending up to several hundred
meters. Such feats of olfactory orientation are impressive when com-
pared with old notions that birds cannot smell, but they nevertheless
represent relatively simple forms of orientation. All require only a search
of the area immediately surrounding the odor source, or at most a
sustained upwind flight response, until the odor source is located. Let
us now turn our attention to the possibility that odors may also be used
during the more difficult tasks of compass orientation and true navi-
gation.
5.2. Can Odors Provide a Reliable Compass?

The function of a compass is to extract directional information
from the environment. Reliable compasses must therefore be based on
environmental phenomena that exhibit a high degree of temporal and
spatial stability, thus permitting a consistent interpretation of directions

from one geographic location to another. A magnetic compass, for ex-
ample indicates the same direction for North regardless of whether it
is used at 40° N latitude of 40° S latitude. Likewise, patterns of star
rotation provide the same compass information everywhere in a given
hemisphere, as does the movement of the sun when coupled with an
internal sense of time. The question of whether odors might also provide
a reliable compass mechanism for orienting birds thus hinges on the
degree of directional stability exhibited by airborne odors. The exis-
tence of highly stable directional odors is rare in the atmosphere due
to the continuously shifting winds usually associated with synoptic
weather features (see Section 4.2). There are, however, a few atmo-
spheric phenomena that are capable of producing highly regular wind
patterns over limited geographical areas. One such example is the sea
breeze effect commonly observed along extended coastlines.
Sea breezes are generated by the differential heating of land and
water. Because of its higher capacity for heat storage and more efficient
thermal mixing, water does not change temperature as rapidly during
heating and cooling as does soil or rock. Land areas, therefore, heat
faster than adjacent bodies of water, and the excess heat is transferred
rapidly to the surface layer of air directly above. Relative to the cooler
air over adjacent water, this warm air rises, decreasing the surface
pressure over the land but raising the pressure aloft (Fig. 5). Because
air always moves from high- to low-pressure areas, the warm air ac-
cumulating aloft over the land moves out to sea, eventually resulting
in a buildup of high pressure over the water's surface. Since this surface
air is now at a higher pressure than air at an equivalent height over
land, surface air tends to move onshore, creating a sea-breeze front.
Depending on the strength of the atmospheric heating conditions and
sea surface temperatures that drive them, sea-breeze fronts can pene-
trate 45-85 km inland along some coastlines (Simpson et al., 1977).
These fronts carry a distinctive signature of odors associated with the
sea and do so in association with regular predictable winds. The result
is the creation of a strong and stable directional odor cue (Waldvogel,
1987). Birds that live in such coastal environments could theoretically
take advantage of this directional olfactory axis as a compass analogous
to the use of star rotation patterns by nocturnal migrants. For example,
a bird that has learned that ocean smells occur in association with a
wind blowing from the west would know that flying crosswind with
the wind at its left results in northward movement. It is important to
note, however, that the differential cooling of land and water favors
changes in the patterns of rising air as day turns to night. Thus, the
BEFORE HEATING
L L
980
984
988
992
996
H
AFTER HEATING
984
~
L H
988
992
996
FIGURE 5. Atmospheric mechanisms responsible for coastal sea breezes. Before sunrise
and heating of the land occurs, vertical profiles of equal pressure (given in millibars) are
the same over land and water. After sunrise, rapid heating of surface air over the land
relative to surface air over water causes a redistribution of high (H) and low (L) pressure
centers. These pressure changes drive both vertical (double arrows) and horizontal (single
arrow) air movements, creating an onshore breeze near the surface. See text for details.
direction of sea breezes changes diurnally, and birds which attempt to

use an olfactory compass must make adjustments for such variations.
No direct test of the possibility that birds might use olfaction as a
compass cue has been attempted. However, indirect evidence that sea-
breeze olfactory mechanisms may operate comes from work performed
with homing pigeons along the west coast of Italy (Ioale et al., 1978;
loale, 1980). The experiments, originally designed to examine the role
of olfaction in forming the navigational map of pigeons (see Section
Ambient Winds
FIGURE 6. Schematic top view of corri-

dor lofts equipped with electric fans that
alter natural wind flow. Solid lines de-
Reversed Control Enhanced note walls made of glass, dashed line in-
dicates wind-permeable screening. In the
central corridor, the birds (controls) re-
ceive ambient air blowing naturally along
the corridor axis. In the enhanced treat-
ment, birds receive winds blowing in the
natural direction but which are generated
by a fan (solid bar) located at one end of
their corridor. Birds in the reversed treat-
ment receive fan-generated air blowing
opposite the natural direction. See text
for further details. (After Ioale et a1., 1978.)
5.3), used special fan lofts that enhanced or reversed the flow of natural
winds (Fig. 6). The corridors of these lofts were oriented along an axis
parallel to the prevailing west-east sea breeze and were equipped to
sense wind velocity and direction electronically. When natural winds
along the corridor axis reached a threshold velocity of 2.5 m/sec the
fans automatically engaged and either enhanced the original wind flow
or reversed it. Testing of the birds' orientation took place after 200-400
hr of exposure to the fan treatment. Control groups oriented in a home-
ward direction when released either to the east or the west of the loft
(Le., parallel to the fan axis), while the experimental groups tended to
orient opposite of home. In tests performed to the north and south (Le.,
perpendicular to the fan axis), both treatment groups were well oriented
in essentially the homeward direction, suggesting that the odor cues
involved in this effect did not influence the birds' efforts to orient from
the north or the south. While these results have been interpreted by
Ioale and co-workers as supportive of an olfactory map sense in homing
pigeons, they can also be accounted for as an orientation response based
on the use of a learned olfactory compass. Unfortunately, a comparable
experiment that trains birds to winds blowing along a north-south axis
has not been performed. Since sea breeze fronts are a prominent at-
mospheric feature of many coastal areas around the world, additional

research expressly designed to examine the possibility that odors might
serve as a useful compass cue would certainly fill an important gap in
the study of avian olfactory orientation.
5.3. True Olfactory Navigation

Unlike the relatively simple upwind orientation exhibited by pro-
cellariids using olfactory landmarks during foraging, the use of odor
cues for true navigation requires a much more sophisticated behavioral
response on the part of birds. Olfactory signals in the environment must
somehow be woven into a two- or three-dimensional navigational map
whose properties should include temporal and spatial constancy (or at
the very least highly predictable variability), relative physiological ease
of detection, and a reasonable degree of spatial resolution (Le., a few
kilometers or less). This map must also allow for accurate position-
fixing and navigation from any direction with respect to the goal with-
out the need to detect odors emanating from the goal itself.
The bird that has received the most attention as a candidate for
using true olfactory navigation is the homing pigeon, although Euro-
pean Starlings (Wallraff and Hund, 1982) and Common Swifts (Apus
apus) (Fiaschi et al., 1974) have also been tested in deprivation studies
akin to those performed by Grubb (1974) on nesting Storm Petrels.
Scores of papers on the topic of pigeon olfactory navigation have ap-
peared since a mechanism was first proposed for its use by Italian
pigeons (Papi et al., 1972). Recent reviews of this work by Papi (1986)
and Schmidt-Koenig (1987) give a flavor for the controversy regarding
the interpretation of data from olfactory navigation experiments with
pigeons. Since this section cannot possibly cover all the experiments
at length, it instead highlights representative examples from tests that
provide evidence both for and against the existence of an olfactory map
sense in homing pigeons. The experiments fall into one of three cate-
gories:
1. Tests involving noninvasive olfactory deprivation or the use of
artificial odors
2. Tests that manipulate natural wind directions at the home loft
3. Tests employing mechanical, chemical, or surgical intervention
of the olfactory system
The original hypothesis of pigeon olfactory navigation is referred
to as the mosaic model; it suggests that young pigeons learn a mosaic
of unique environmental odors while growing up at their home loft.
Thus, a map develops based on direct experience with odors encoun-

tered at the loft as well as those experienced during exercise and train-
ing flights. More distant odors brought to the loft by prevailing winds
can also be incorporated into such a map. While this kind of map can
conceivably operate over distances of many tens of kilometers, its use
is necessarily limited to areas in which the bird has had some direct
experience with local or wind-borne cues. In other words, because of
the unique construction of a mosaic, it is not usually possible to ex-
trapolate odor patterns learned in the vicinity of the home loft to areas
located hundreds of kilometers away. A second, or gradient, model
(Wallraff, 1980a, 1981) overcomes this distance limitation by assuming
the existence of very long-range atmospheric odor gradients that are
stable in time and space. A pigeon could use these gradients to fix its
position at distances well beyond previous flight experience by com-
paring the observed odorant concentration at its current position with
the remembered value of the gradient at the home loft. As pointed out
by Schmidt-Koenig (1987), these two olfactory map models often make
different predictions about the response of pigeons to certain types of
experimental manipulations. This is a result of the different require-
ments of the two models: the gradient model requires that birds make
quantitative judgments about environmental odors in order to "read"
their map, while the mosaic model necessitates only a qualitative dis-
crimination among odor cues.
A variety of. tests have attempted to manipulate the presumptive
olfactory map sense in pigeons by either (1) training birds to artificial
odor cues, or (2) presenting a misleading olfactory stimulus during
transport to the release site or at the site itself. Benvenuti et 01. (1973a)
applied a-pinene, olive oil, and a plant extract mixture to the beaks of
pigeons before release and found disorientation among all three treat-
ments compared with untreated controls. Keeton and Brown (1976),
however, were unable to repeat these results using a-pinene applied
to the beaks of homing pigeons in the United States. Papi et 01. (1974)
raised birds in a fan loft with glass-walled wind tunnels in which the
birds received daily training to artificial directional odors. One group
received moving air generated by fans that blew the scent of olive oil
from the west and the odor of terpentine from the east, while a phys-
ically separate second group received the opposite odor treatment. When
released out of sight of their lofts, the two groups oriented in opposite
directions when one of the two olfactory test stimuli was applied to
their beaks. Once again, this experiment could not be repeated with
pigeons in the United States (D. B. Quine and J. A. Waldvogel, unpub-
lished data).
OLFACTORY ORIENT AnON 303
,. . . . . .,. . . ,. . ".!. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ·t·. . . . . . . . -

FIGURE 7. Outward journey de-
tour test design, showing the route
of travel and predicted orienta- Hypathc-llcaJ Odor Oradlc:ftl
.................. " .... ,. -.. ,........... ,....................."'............... ............................, -...........-.
Nonh ~ Soalli
~
tion response for two identical

groups of pigeons (A and B)
transported to a north release site.
Under the mosaic map hypoth-
esis, each group encounters dif-
ferent olfactory stimuli during the
initial leg of the journey (shaded
and hatch ed areas), which takes
group A to the west and group B
to the east. At the north rel ease
site, their orientation reflects this
initial displacement, resulting in
group A's h eading east and group
B's heading west. If, however, a
gradient map (dashed lines) forms
the basis of pigeon navigation ,
each group perceives th e same
northward displacement and ori-
ents to the south, in the home-
ward direction.
Tests involving olfactory "detours" during transport from the home

loft to the release site have also been performed at lofts in Italy, Ger ..
many, and the United States. This experiment requires taking two groups
of birds to a common release site along widely divergent paths, such
that the initial leg of the outward journey is essentially opposite for
each treatment (Fig. 7) . Here a difference arises between the predicted
results of the mosaic and gradient models. If the initial leg of the out ..
ward journey is important for the accurate reading of a mosaic map,
each treatment should orient opposite the other upon release, since
they will have perceived opposite displacements from home. If, on the
other hand , detecting the concentration gradient of an odor at the release
site is the important step in assessing position relative to the loft, the
detour should have little or no effect on orientation or homing. (No
effect of the detour might also indicate no influence of olfaction on the
map in any fashion.) Repeated releases from certain sites in Italy suggest
the presence of a detour effect (Papi et 01., 1973; Papi, 1976), but there
are no unequivocal data to indicate that it has a purely olfactory basis.
Attempts to replicate these results in Germany and the United States
have failed to show a reliable effect (Keeton, 1974b; Fiaschi and Wagner,
1975; Hartwick et 01., 1978; Papi et 01., 1978b; Wallraff, 1980a). Very
recent modifications of this detour experiment have been performed
by Kiepenheuer (1985, 1986) and by Benvenuti and Wallraff (1985) in

which false-release site odors and outward journey air samples have
been manipulated. Using various combinations of free access to envi-
ronmental air, bottled air, and air samples taken from random locations,
it has been shown that, at least in Germany, one may be able to induce
random or misdirected orientation using a false olfactory message. Po-
tential problems with these experiments include the observation that
homing success is not usually significantly affected by the odor treat-
ments (indicating that the orientation effects are transient), and also
that the input of other potential orientation cues (e.g., magnetism) has
not been completely ruled out. Initial tests with false release site odors
and "nonsense" odors have also recently been performed in the United
States, with preliminary results again suggesting little or no effect of
odors on orientation or homing success (J. B. Phillips, R. Madden, and
J. A. Waldvogel, unpublished data).
Only one field test has been conducted with homing pigeons to
determine the physical characteristics of relevant navigational odors.
Wallraff and Foa (1981) used fiberglass and charcoal filters to trap air-
borne particles ranging in diameter from 0.04 to 2.0 JLm before this air
was pumped into containers used to transport pigeons. In tests con-
ducted 24-155 km from the home loft in Germany, the orientation was
significantly poorer for the birds transported with filtered air than it
was for unfiltered air controls. While this suggests olfactory involve-
ment in orientation and homing, it is not clear whether the odors are
being used as a direct cue for navigation or serve merely as a motiva-
tional factor that acts to focus the bird's attention on other navigational
cues. Because of the apparent variability in olfactory response between
birds from different countries, similar tests need to be carried out at
lofts in Italy and the United States, at a wider variety of distances from
the home loft, and with more specialized filters or aerosol traps to
determine precisely the nature of odorants that might be of interest to
pigeons.
A second category of pigeon olfactory navigation experiments in-
cludes tests that use differentially shielded aviaries to alter natural
windflow in some predictable manner. Several very ingenious loft de-
signs have been employed to manipulate the olfactory environment
around pigeons, and I will begin by discussing studies involving de-
flector lofts. First used by Baldaccini et 01. (1975), deflector lofts are
cube-shaped cages made of vertically aligned wooden slats that permit
windflow through the loft. A control loft consists of this wind-perme-
able cage only, while the experimental lofts have attached to all four
corners large deflecting panels, the lower portions of which are made
CONTROL
x x x
1
1"""""""":
i lill 1111 1III 1lII i
~.J/
"V
""""01 1101
y
1 y y
1 mil"
FIGURE 8. Schematic top view of deflector lofts. Each loft consists of a cube-shaped
cage with wind-permeable sides (dashed lines). The two experimental lofts have attached
to their corners large deflector panels angled at 45° with respect to the cage walls. The
panels of one loft cause a clockwise (eW) rotation of winds and their associated odors
(e.g., X and V), while the other produces counterclockwise (CCW) rotation of winds and
odors. The control loft (C) lacks deflector panels and does not alter natural wind flow.
of wood and the upper portions Plexiglas (Fig. 8). The 45° angle made
by the deflector panels of one loft creates a clockwise (CW) rotation of
winds, while the reverse positioning of another set of panels located
on a second loft rotates winds counterclockwise (CCW) relative to the
control condition. Both olfactory hypotheses predict that birds raised
in deflector lofts should acquire rotated olfactory maps, one set of birds
with a CW bias, the other CCW. As predicted, when pigeons are raised
in these lofts from the time of fledging (~5 weeks posthatching) until
they are 15-20 weeks of age, those that live in the CW loft exhibit a
clockwise bias of initial orientation compared to control birds, while
those from the CCW loft orient counterclockwise. Unlike the results of
many other olfactory experiments, consistent and striking effects of
residence in the deflector lofts have been observed in all countries in
which tests have been conducted, making this effect one of the most
repeatable experiments ever designed to examine olfactory navigation
in pigeons (Baldaccini et al., 1975; Kiepenheuer, 1978; Waldvogel et
al.,1978).
However, subsequent deflector loft experiments in Germany and
the United States have raised doubts about whether the effect really
has its basis in olfaction, or even its influence on a navigational map.

Working with deflector loft birds in Germany, Kiepenheuer (1979) showed
that temporary chemical anesthesia of the olfactory mucosa has no
affect on the birds' strong orientation bias. This result is not predicted
by either olfactory model, since a sudden inactivation of the sensory
channel used to read the map should result in random orientation and
poor homing success. Wallraff (1980b) dismisses this problem by in-
voking a preferred compass direction (PCD) effect to explain Kiepen-
heuer's results, suggesting that the birds transfer their biased map in-
formation over to a compass mechanism that would not be affected by
the chemical anesthesia. This PCD explanation is not universally ac-
cepted, however, as discussed by Phillips and Waldvogel (1982) and
Schmidt-Koenig (1987). In addition, Waldvogel and Phillips (1982),
working in the United States, showed that, when tested under complete
overcast, the deflector loft effect disappears in American pigeons. Since
the American birds remain well oriented toward home under overcast,
these results suggest that the deflector loft effect probably has its basis
in some alteration of the birds' sun compass rather than an odor map.
But similar releases conducted with German birds did not demonstrate
an effect of overcast on the orientation bias of permanent-resident de-
flector loft pigeons (Kiepenheuer, 1982).
Baldaccini et a1. (1978) demonstrated that deflector loft birds who
are raised as one treatment, for example CW, can be convinced to switch
their bias to CCW after several weeks of living in their loft with the
deflector panels repositioned to reverse the original pattern of wind
rotation. This indicates that the deflector loft effect does not result in
a permanent alteration of an odor map but rather represents an ad-
justable response to major changes (perhaps olfactory) in the birds'
environment. Using a modification of the original deflector loft tech-
nique, Waldvogel et a1. (1980) showed that the deflector loft effect can
in fact be generated after as little as 7 days exposure to an altered wind
environment, using experienced American birds whose permanent home
is other than the deflector lofts. This so-called short-term deflector loft
effect has now become an important part of experiments that seem to
show a nonolfactory basis for the deflector loft effect in the United
States (Phillips and Waldvogel, 1982; Waldvogel et aI., 1988). Recent
criticism by Papi (1986) that the short-term deflector loft effect does
not constitute a challenge to the olfactory model overlooks the fact that
when given the choice between rotated odor cues and altered polarized
light patterns, the birds respond by indicating that optical cues are the
more important parameter in generating their orientation bias. This is
not to say, however, that the entire deflector loft picture might not be
OLFACTORY ORIENT A nON a07
a complex one for American pigeons. On the one hand, the short-term
deflector loft effect appears to result from the birds viewing abnormal
patterns of polarized light that cause them to miscalibrate their sun
compass (Phillips and Waldvogel, 1982, 1988), while on the other hand
permanent-resident deflector loft birds do not respond to light cues
when presented with the same optical environment used in short-term
deflector loft tests (Waldvogel and Phillips, 1982), a finding consistent
with an olfactory interpretation of the deflector loft effect. In efforts to
sort out these apparently paradoxical data, it is important to remember
that deflector lofts always rotate winds regardless of any other manip-
ulations made to the lofts or the birds. If olfaction is fundamental to
pigeon homing, as has been repeatedly claimed (see Papi, 1976, 1986),
a bird living in these lofts must incorporate a bias into its olfactory
map by virtue of the altered olfactory world with which it is forced to
deal. As a result, any kind of evidence which shows that birds who
live in the deflector lofts do not pay attention to olfactory cues should
be considered an important exception to the predictions generated by
both olfactory models of pigeon homing.
Recent tests in Italy using deflector loft birds that have been sub-
jected to sectioning of the anterior commissure have further compli-
cated any simple interpretation of the deflector loft effect (Foa et al.,
1986). With the assumption that olfactory information from one nostril
is probably transferred between cerebral hemispheres via the anterior
commissure, a test was made of whether birds lacking the ability for
olfactory lateralization between hemispheres could build more than
one odor map. When housed in the CW loft the commissurotomized
birds had their right nostril plugged, and when residing in the CCW
loft their left nostril was occluded. The birds were alternated between
each loft type for a total of 69 days, remaining in either the CW or CCW
loft for 3 days at a time. When released with the right nostril plugged,
the birds exhibited a clockwise bias of initial orientation, while those
with an occluded left nostril oriented counterclockwise. No deflection
was observed when the birds were kept for an equivalent time in a
normal aviary. These intriguing results (as yet unreplicated in either
Germany or the United States), while indicating that multiple olfactory
maps might exist in the pigeon brain, are nevertheless still consistent
with the idea that nonolfactory cues may instead cause the deflector
loft effect. For example, if the Italian commissurotomized deflector loft
birds had been raised in only one of the two types of deflector lofts
with only a single nostril plugged and were then tested with the op-
posite nostril occluded, the olfactory model would predict disorien-
tation, while the polarized light model would predict an appropriate
r 1 meter
----
111
FIGURE 9. Diagrammatic top view of a differentially shielded aviary used in experiments
to test olfactory navigation by homing pigeons. Solid lines represent Plexigas walls which
form a corridor, the open ends of which are covered by wind-permeable screening (dashed
lines). The birds are housed between these screened walls where they have access only
to winds blowing along the corridor axis. One loft has its axis of wind acceptance aligned
North-South, while the complimetnary loft accepts winds along an East-West axis.
Groups of birds are raised from the time of fledging in these lofts and their orientation
then tested from distant release sites in all four cardinal compass directions. (After Ioale,
1982.)
deflection. Thus, the commissurotomy experiment as performed by Foa

and colleagues proves only that the orientation mechanisms of pigeons
are highly malleable and capable of making rather unusual adjustments.
It is therefore difficult to conclude on the basis of these data that the
observed effect is solely olfactory or optical in nature, and it remains
unclear whether olfaction or polarized light universally forms the basis
for the deflector loft effect, or whether the effect is caused by odors in
Italy and optical cues in the United States.
Other studies using differentially shielded aviaries have also been
conducted. Ioale (1982) raised birds in special corridor lofts that permit
only limited access to natural windflow (Fig. 9). In one set of lofts,
natural winds could enter from either the east or the west, but not the
north and south, while in another set the axis of wind acceptance was
north-south only. When tested from the four cardinal compass direc-
tions, all groups of birds oriented toward home from directions cor-
responding to the wind axis sensed in their loft, with birds raised in
OLFACTORY ORIENT ATION 309
the east-west conditions (i.e., the direction of the prevailing winds)

showing better orientation than those raised in the north-south con-
ditions. Homeward orientation was essentially lost in other experi-
ments in which German and Italian birds were raised in lofts screened
from all winds, although effects on homing success were variable (Bal-
daccini et al., 1974; Wallraff, 1979a). In many of these tests, little effort
has been made to control for other possible orientation cues which are
probably also altered by the lofts (such as patterns of polarized light),
and to date no replications of these experiments have been attempted
in the United States.
In studies of olfactory orientation, it is always preferable to design
an experiment in which the investigator manipulates the olfactory world
around the bird while leaving the animal's sensory apparatus intact. If
for no other reason, this convention is desirable because of the difficulty
encountered in controlling the complicating side effects of surgery or
other forms of physiological intervention on the birds' sensory system.
While the results of deprivation experiments are useful and bear di-
rectly on the issue of olfactory navigation, it is critical to remember
that there is also good reason to be cautious about behavioral data
obtained from surgical, mechanical, or chemical intervention. As pointed
out by Wenzel and Rausch (1977) and Wenzel (1983), both histological
and behavioral evidence suggests an intimate link between the anatom-
ical integrity of the olfactory system and normal functioning of other
areas in the avian brain. Thus, for instance, interference with the sense
of smell induced by severing the olfactory nerves causes retrograde
degeneration of neurons in the olfactory bulb, which in turn affects
projections to other brain regions such as the prepiriform cortex, the
parolfactory lobe and the ventral hyperstriatum. Major behavioral dis-
turbances can also be generated upon damage to the olfactory pathway,
including decrements in learning, motivation, and attentional behavior,
all of which conceivably playa role in orientation and navigation (Wen-
zel, 1982).
A large number of olfactory deprivation studies have been con-
ducted on homing pigeons. Deprivation has been induced mechanically
using dental paste and cotton plugs inserted into the bird's nostrils or
by means of hollow plastic tubes that permit seminormal breathing
while at the same time preventing chemical stimulation of the olfactory
mucosa. Temporary odor deprivation has also been achieved chemi-
cally using topical anesthetics (e.g., Xylocaine). Finally, surgical inter-
vention has been used either by itself, as in lesions of the anterior
commissure or bilateral transections of the olfactory nerves, or in com-
bination with mechanical blockage of the olfactory system as in ex-
periments in which unilateral sectioning of the olfactory nerve is com-

bined with a single nasal plug positioned in either the ipsilateral nostril
(control) or contralateral nostril (experimental).
When bilateral sectioning of the olfactory nerve is performed on
Italian birds, vanishing bearings for the experimental treatments tend
to be more scattered than controls. However, the most dramatic effect
is on homing success, especially from unfamiliar release sites (Papi et
a1., 1971, 1972; Benvenuti et a1., 1973b). Similar results have been
obtained in Germany by Snyder and Cheney (1975) using nasal plugs.
Nerve-sectioning and nasal plug tests conducted in the United States
also show a decrement in homing from unfamiliar sites, but the effect
is not as dramatic as that observed in Europe (Keeton et a1., 1977; Papi
et a1., 1978a). The effect of reversible olfactory anesthesia using chem-
icals has been more variable, ranging from clear-cut reduction in ori-
entation and homing ability for Italian birds (laale, 1983), to no effect
on German birds (Wiltschko and Wiltschko, 1987; Wiltschko et a1.,
1987a), and somewhere in between for American pigeons (Papi et a1.,
1978a; Wiltschko et a1., 1987b).
Sectioning of the olfactory nerves is a traumatic operation, and
even when proper surgical controls are used there is always the pos-
sibility that motivation to home has been impaired as well as (or instead
of) the ability to navigate. Despite claims to the contrary (Wallraff,
1979b; Papi, 1986), in my opinion there has never been a satisfactory
resolution to the potential problem of reduced motivation in olfactory
deprivation studies. It is therefore difficult to interpret data from hom-
ing experiments in which birds do not home, mostly because the fate
of the nonhomers is rarely known. In cases in which this information
is available because of recoveries by racing pigeon enthusiasts (Wallraff
et a1., 1981), the time to recovery is still not certain nor are the birds'
actual flight paths known, making it extremely difficult to prove that
the nonhomers flew just as far as the successful homers, only in random
directions.
Comparative studies of olfactory deprivation conducted in differ-
ent countries by Wiltschko et a1. (1987b) have shown that pigeons in
Italy appear to rely on odor cues in a much more fundamental way
than do birds in Germany or in the United States, where little or no
effect of olfactory deprivation is observed. This pattern of regional vari-
ation in the use of olfactory cues, the existence of which is not uni-
versally recognized and occasionally even rejected outright (e.g., Papi,
1986), is also observed in virtually every other type of odor navigation
experiment attempted in all three countries. The pattern may be the
result of atmospheric influences on odor stability and directionality,

which make the Italian coastline a better environment for reliable ol-
factory orientation (Waldvogel, 1987; see also Section 5.2)' or may be
due to genetic variation among populations of birds, although studies
with birds born in one country but raised and tested in another appear
to speak against any profound genetic component which influences a
pigeon's predisposition to use olfactory navigation (e.g., Kiepenheuer
et aI., 1979). Recent work by Wiltschko et a1. (1987c) shows that the
degree to which olfaction is incorporated into a pigeon's orientation
system may also depend largely on early experiences with odor cues.
When raised in a normal partially wind-shielded ground level loft
("German style"), the birds' orientation is not affected by nasal plugs
or chemical anesthesia. However, when raised "Italian style" in a loft
situated atop a multistory building with open access to all winds, these
forms of anosmia cause disorientation. Preliminary tests in the United
States comparing "American-style" rearing techniques and those used
in Italy also indicate that early experiences may be crucial in deter-
mining the extent to which olfactory cues are incorporated into a nav-
igation scheme (S. Benvenuti and A. I. Brown, unpublished data).
Thus, when a wide variety of data are considered, it appears that
olfaction likely plays an important role in the homing behavior of pi-
geons raised in Italian and perhaps certain German lofts but that birds
from other German facilities as well as those in the United States do
not seem to use olfactory cues to any great extent. It therefore appears
that claims by Papi (1982b, 1986) and Wallraff (1980b, 1984) that ol-
faction forms a universal and essential element of pigeon homing must
be considered unsubstantiated at this time. Furthermore, in lieu of the
detailed studies of sensory physiology that are necessary in order to
show an ability for pigeons to detect and discriminate among natural
odors, it seems premature to grant powers of truly long-range olfactory
navigation to the homing pigeon. However, if there is indeed an olfac-
tory basis to pigeon homing in Italy, efforts must be made to elucidate
a reasonable explanation for why odor cues are not attended to by birds
in other geographical areas. Such an explanation must take into account
how the selective incorporation of olfactory information into an other-
wise diverse navigational repertoire can occur (see Keeton, 1974a; Able
and Bingman, 1987) and to what extent patterns of atmospheric stability
are involved in defining the use of odors for navigation. At this stage
of research, it becomes crucial for investigators to design their tests of
olfactory navigation with keen rigor, to be sure that they are examining
a physiologically as well as atmospherically realistic question, and to
minimize the influence of surgical or other harsh physical intervention

into the birds' olfactory system.
6. CONCLUSIONS
Substantial evidence now exists to support the view that birds

possess a functional olfactory system. Clear-cut olfactory responses to
a variety of chemical stimuli have been obtained from a wide range of
species, using established physiological measures. While the number
of species for which absolute olfactory thresholds have actually been
determined is still small, on the basis of these few data, it appears that
avian olfactory sensitivity lies somewhere within the 10- 5 _10- 7 M
range (Le., around the 1-ppm level). This level of sensitivity places
birds near the bottom of the list of vertebrates possessing moderate
olfactory sensitivities but is apparently sufficient to permit the detection
and use of environmental odors as orientation cues. There is still a
serious need for additional work on the sensitivity of birds to natural
odors, their perceptual thresholds for the discrimination of these odors,
as well as the ambient concentrations and chemical properties of nat-
ural odor sources.
Atmospheric processes and their role in shaping the dispersion of
natural odors are seen as important elements influencing the ease with
which birds can use olfactory cues for orientation. Processes ranging
in scale from simple molecular diffusion to long-range synoptic trans-
port all have an effect on odor availability in the environment, and
each works in different ways to influence the utility of odors as ori-
entation cues. Some useful gain is made in understanding the influences
of these atmospheric factors when odor transport is analyzed by means
of mathematical equations derived from work on insect pheromone
signaling and long-range transport of pollutants, but too many physical
and physiological aspects of what constitute relevant environmental
odors for birds remain unknown for us to apply these equations broadly.
It is therefore premature to predict accurately the precise limits of avian
olfactory orientation behavior.
Behavioral evidence indicates that some species of birds are able
to localize nearby sources of food and nesting materials using olfactory
cues, while other species use odors to detect food and possibly nest
sites from distances of several tens or even hundreds of meters. This
form of landmark orientation is by far the most commonly observed
use of olfaction by birds, although the intriguing possibility that pher-
omones may mediate aspects of avian reproductive biology could prove

more ubiquitous, if true. Furthermore, data from studies of olfactory
landmark orientation in birds clearly demonstrate that no longer is it
realistic to assume a low level of olfactory sensitivity in birds possessing
small olfactory neural structures. Examples of accurate olfactory ori-
entation in groups with robust olfactory systems (e.g., vultures, kiwis,
and procellariids) are no more common than those from birds with
relatively small olfactory equipment (e.g., magpies, tits, and starlings).
The issue of whether odors form the basis of a compass or navi-
gational map in birds (especially homing pigeons) remains unsettled,
although in my opinion the bulk of the evidence is currently against
an essential role for odors in avian navigation. There is mounting evi-
dence that olfaction may be used as a regional component of the pi-
geon's otherwise diverse repertoire of navigational mechanisms, as evi-
denced by the fact that American and some German homing pigeons
do not appear to rely much on odors, while other pigeons in Germany
as well as Italian birds seem to pay considerable attention to odor cues.
Whether this geographical specificity in olfactory response is the result
of genetic predisposition or behavioral experience awaits the result of
international cross-fostering experiments now in progress. In addition,
by applying training techniques in which birds receive widely different
forms of early olfactory experience to other established experimental
procedures for testing odor navigation in pigeons (e.g., false-release site
experiments or studies involving olfactory deprivation), useful infor-
mation should be gained about regional and genetic differences in the
use of olfactory orientation. The possibility that an atmospheric expla-
nation such as the sea-breeze phenomenon could help explain the dif-
ferences between data from otherwise identical olfactory navigation
experiments conducted in the United States and in Italy raises a need
for the testing of American birds in meteorological conditions closely
resembling those of the Italian peninsula. The west central coast of
Florida suggests itself immediately as a possible location for such tests.
More important, however, is the need for a critical reexamination
of approaches to the study of olfactory navigation. A new research
emphasis on the problem is required if nagging questions about phys-
iological sensitivity to odors or the atmospheric realities of olfactory
orientation are to be answered. Tests that clearly delineate between
motivational and orientational influences in olfactory navigation should
become the standard against which new experiments are judged. In
short, we should strive to create a research environment of cooperation
and objective evaluation of data from a wide variety of experiments
that will do justice to the realities of olfactory influences on avian
orientation. If this can be achieved, we will likely be rewarded by a

much greater appreciation of the role that odors play in bird behavior.
ACKNOWLEDGMENTS. Many people assisted in the preparation of this

chapter. I thank Douglas Paine for help with the mechanisms of at-
mospheric transport and Daniel McNaughton for information on sources
of biogenic odors. Other, including Irene Brown, Nancy Clum, Stephen
Nowicki, Susan Peters, John Phillips, and Charles Walcott, critically
reviewed an earlier version of the manuscript. Their comments have
greatly improved the content and readability of this chapter.
REFERENCES
Able, K. P., 1980, Mechanisms of orientation, navigation, and homing, in: Animal Mi-
gration, Orientation, and Navigation (S. A. Gauthreaux, Jr., ed.). Academic, New
York, pp. 283-373.
Able, K. P., and Bingman, V. P., 1987, The development of orientation and navigation
behavior in birds, Q. Rev. BioI. 62:1-29.
Adams, D. F., Farwell, S. 0., Pack, M. R., and Robinson, E., 1981a, Biogenic sulfur gas
emissions from soils in Eastern and Southeastern United States, J. Air Pollut. Cont.
Assoc. 31:1083-1089.
Adams, D. F., Farwell, S. 0., Robinson, E., Pack, M. R., and Bamesberger, W. 1., 1981b,
Biogenic sulfur source strengths, Environ. Sci. Technol. 15:1493-1498.
Archer, A. L., and Glen, R. M., 1969, Observations on the behaviour of two species of
honeyguides, L. A. County Mus. Contrib. Sci. 160:1-6.
Audubon, J. J., 1826, Account of the habits of the turkey buzzard, Vultur aura, particularly
with the view of exploding the opinion generally entertained of its extraordinary
power of smelling, Edinb. New Phil. J. 2:172-184.
Baldaccini, E. N., Benvenuti, S., Fiaschi, V., loale, P., and Papi, F., 1974, Pigeon navi-
gation: Effects of manipulation of sensory experience at home site, ]. Compo Physiol.
94:85-96.
Baldaccini, E. N., Benvenuti, S., Fiaschi, V., and Papi, F., 1975, Pigeon navigation: Effects
of wind deflection at home cage on homing behaviour, ,. Compo Physiol. 99:177-186.
Baldaccini, E. N., Benvenuti, S., Fiaschi, loale, P., and Papi, F. 1978, Investigation of
pigeon homing by means of "deflector cages," in: Animal Migration, Navigation,
and Homing (K. Schmidt-Koenig and W. T. Keeton, eds.). Springer-Verlag, Berlin,
pp.78-91.
Balthazart, J., and Schoffeniels, E., 1979, Pheromones are involved in the control of sexual
behavior in birds, Naturwissenschaften 66:55-56.
Bang, B. G., 1960, Anatomical evidence for olfactory function in some species of birds,
Nature (Lond.) 188:547-549.
Bang, B. G., 1971, Functional anatomy of the olfactory system in 23 orders of birds, Acta
Anat. Suppl. 79:1-76.
Bang, B. G., and Cobb, S., 1968, The size of the olfactory bulb in 108 species of birds,
Auk 85:55-61.
Bang, B. G., and Wenzel, B. M., 1985, Nasal cavity and olfactory system, in: Form and
Function in Birds, VoL 3 (A, S, King and J. McLelland, eds.), Academic, New York,
pp. 195-225.
Becker, j., and van Raden, H., 1986, Meteorologische Gesichtspunkte zur olfaktorischen
Navigationshypothese, J. Ornithol. 127:1-8.
Benham, W. B., 1906, The olfactory sense in Apteryx, Nature (Lond.) 74:222-223.
Benvenuti, S., and Wallraff, H. G., 1985, Pigeon navigation: Site stimulation by means
of atmospheric odours, J. Compo Physiol. A 156:737-746.
Benvenuti, S., Fiaschi, V., Fiore, 1., and Papi, F., 1973a, Disturbances of homing behaviour
in pigeons experimentally induced by olfactory stimuli, Monit. Zool. Ital. (N.S.) 7:
117-128.
Benvenuti, S., Fiaschi, V., Fiore, 1., and Papi, F., 1973b, Homing performances of in-
experienced and directionally trained pigeons subjected to olfactory nerve section,
J. Compo Physiol. 83:81-92.
Bossert, W. H., and Wilson, E. 0., 1963, The analysis of olfactory communication among
animals, J. Theor. Biol. 5:443-469.
Buitron, D., and Nuechterlein, G. 1., 1985, Experiments on olfactory detection of food
caches by black-billed magpies, Condor 87:92-95.
Clark, 1., and Mason, J. R., 1985, Use of nest material as insecticidal and anti-pathogenic
agents by the European starling, Oecologia 67:169-176.
Clark, 1., and Mason, J. R., 1987, Olfactory discrimination of plant volatiles by the
European starling, Anim. Behav. 35:227-235.
Cobb, S., 1960a, A note on the size of the avian olfactory bulbs, Epilepsia 1:394-402.
Cobb, S., 1960b, Observations on the comparative anatomy of the avian brain, Perspect.
Biol. Med. 3:383-408.
Davis, R. G., 1973, Olfactory psychophysical parameters in man, rat, and pigeon, J. Compo
Physiol. Psychol. 85:221-232.
Dawson, G. A., 1977, Atmospheric ammonia from undisturbed land, J. Geophys. Res. 82:
3125-3133.
Eliasson, A., 1980, A review of long-range transport modelling, J. Appl. Met. 19:231-240.
Elkinton, j. S., and Carde, R. T., 1984, Odor dispersion, in: Chemical Ecology of Insects
(W. J. Bell and R. T. Carde, eds.), Sinauer, Sunderland, pp. 73-91.
Emlen, S. T., 1975, Migration: orientation and navigation, in: Avian Biology, Vol. 5
(D. S. Farner and J. R. King, eds.), Academic, New York, pp. 129-219.
Engen, T., 1987, Remembering odors and their names, Am. Sci. 75:497-503.
Eriksson, E., 1963, The yearly circulation of sulfur in nature, 1. Geophys. Res. 68:4001-4008.
Ferber, G. j., Heffter, j. 1., Draxler R. R., Lagomarsino, R. J., Thomas, F. 1., Dietz, R. N.,
and Benkovitz, C. M., 1986, Cross-Appalachian Tracer Experiment (CAPTEX '83)
finol report, National Oceanic and Atmospheric Administration Technical Memo-
randum ERL ARL-142, Washington, D. C.
Fiaschi, V., and Wagner, G., 1976, Pigeon homing: Some experiments for testing the
olfactory hypothesis, Experientio 32:991-993.
Fiaschi, V., Farina, A., and loale, P., 1974, Homing experiments on swifts Apus opus
(1.) deprived of olfactory perception, Monit. Zoo I. Itol. (N.S.) 8:235-244.
Fletcher, T. C., 1981, Non-antibody molecules and the defense mechanisms of fish, in:
Stress and Fish (A. D. Pickering, cd.), Academic, New York, pp. 171-183.
Foa, A., Bagnoli, B., and Giongo, F., 1986, Homing pigeons subjected to section of the
anterior commissure can build up two olfactory maps in the deflector lofts, 1. Compo
Physiol. A 159:465-472.
Friedmann, H., and Kern, J., 1956, The problem of cerophagy or wax-eating in the honey-
guides, Q. Rev. BioI. 31:19-30.
Goldsmith, K. M., and Goldsmith, T. H., 1982, Sense of smell in the Black-chinned
Hummingbird, Condor 84:237-238.
Gotaas, Y., 1980, OECD programme on long-range transport of air pollutants-measure-
ments from aircraft, Ann. NY Acad. Sci. 338:453-462.
Gould, J. 1., 1982, The map sense of pigeons, Nature (Land.) 296:205-211.
Graedel, T. E. 1978, Chemical Compounds in the Atmosphere, Academic, New York.
Griffin, D. R., 1955, Bird navigation, in: Recent Studies in Avian Biology (A. Wolfson,
ed.), University of Illinois Press, Urbana, pp. 154-197.
Grubb, T. c., Jr., 1972, Smell and foraging in shearwaters and petrels, Nature (Lond.)
237:404-405.
Grubb, T. C., Jr., 1974, Olfactory navigation to the nesting burrow in Leach's petrel
(Oceanodroma leucorrhoa), Anim. Behav. 22:192-202.
Hara, T. J., 1975, Olfaction in fish, Prog. Neurobiol. 5:271-335.
Hartwick, R., Kiepenheuer, J., and Schmidt-Koenig, K., 1978, Further experiments on the
olfactory hypothesis of pigeon homing, in: Animal Migration, Navigation, and Hom-
ing (K. Schmidt-Koenig and W. T. Keeton, eds.), Springer-Verlag, Berlin, pp. 107-118.
Henton, W. W., 1969, Conditional suppression to odorous stimuli in pigeons, J. Exp.
Anal. Behav. 12:175-186.
Hitchcock, D. R., 1976, Atmospheric sulfates from biological sources, J. Air Pollut. Contf.
Assoc. 26:210-215.
Houston, D. c., 1984, Does the King Vulture Sarchorhamphus papa use a sense of smell
to locate food?, Ibis 126:67-69.
Hutchison, 1. V., and Wenzel, B. M., 1980, Olfactory guidance in foraging by procellar-
iiforms, Condor 82:314-319.
Hutchison, 1. V., Wenzel, B. M., Stager, K. E., and Tedford, B. 1., 1984, Further evidence
for olfactory foraging by Sooty Shearwaters and Northern Fulmars, in: Marine Birds:
Their Feeding Ecology and Commercial Fisheries Relationships (D. N. Nettleship,
G. A. Sanger, and P. F. Springer, eds.), Special Publication Canadian Wildlife Service,
Ottawa, pp. 72-77.
loale, P., 1980, Further investigations on the homing behaviour of pigeons subjected to
reverse wind direction at the loft, Manit. Zool. Ital. (N.S.) 14:77-87.
loale, P., 1982, Pigeon homing: Effects of differential shielding of home cages, in: Avian
Navigation (F. Papi and H. G. Wallraff, eds.), Springer-Verlag, Berlin, pp. 170-178.
loale, P., 1983, Effects of anaesthesia of the nasal mucosae on the homing behaviour of
pigeons, Z. Tierpsychol. 61:102-110.
loale, P., Papi, F., Fiaschi, V., and Baldaccini, N. E., 1978, Pigeon navigation: Effects
upon homing behaviour by reversing wind direction at the home loft. J. Camp.
Physiol. 128:285-295.
Jacob, J., Balthazart, J., and Schoffeniels, E., 1979, Sex differences in the chemical com-
position of uropygial gland waxes in domestic ducks, Biochem. Sys. Ecol. 7:149-153.
James, P. C., 1986, How do Manx Shearwaters Puffinus puffinus find their burrows?,
Ethology 71:287-294.
Jarvi, T., and Wiklund, C., 1984, A note on the use of olfactory cues by the great tit Parus
major in food choice, Fauna Norv. Ser. C 7:139.
Josephson, D. B., and Lindsay, R. C., 1986, Enzymic generation of volatile aroma com-
pounds from fresh fish, in: Biogeneration of Aromas (T. H. Parliment and R. Croteau,
eds.), American Chemical Society, Washington D. C., pp. 201-219.
Jouventin, P., 1977, Olfaction in Snow Petrel. Condor 79:498-499.
Jouventin, P., and Robin, J. P., 1984, Olfactory experiments on some Antarctic birds, Emu
84:46-48.
Keeton, W. T., 1974a, The orientational and navigational basis of homing in birds, Adv.
Std. Behav. 5:47-132.
Keeton, W. T., 1974b, Pigeon homing: No influence of outward journey detours on initial
orientation, Monit. Zool. Hal. (N.S.) 8:227-234.
Keeton, W. T., and Brown, A. I., 1976, Homing behavior of pigeons not disturbed by
application of an olfactory stimulus, J. Compo Physiol. 105:252-266.
Keeton, W. T., Kreithen, M. 1., and Hermayer, K. L., 1977, Orientation of pigeons deprived
of olfaction by nasal tubes, J. Camp. PhysioJ. 114:289-299.
Kennedy, R. J., 1971, Preen gland weights, Ibis 113:369-372.
Kennedy, J. S., and Marsh, D., 1974, Pheromone-regulated anemotaxis in t1ying moths,
Science 184:999-1001.
Kiepenheuer, J., 1978, Pigeon homing: A repetition of the det1ector loft experiment, Behav.
EcoJ. SociobioJ. 3:393-395.
Kiepenheuer, J., 1979, Pigeon homing: Deprivation of olfactory information does not
affect the det1ector effect, Behav. Ecol. SociobioJ. 6:11-22.
Kiepenheuer, J., 1982, Pigeon orientation: A preliminary evaluation of factors involved
or not involved in the det1ector loft effect, in: Avian Navigation (F. Papi and H. G.
Wallraff, eds.), Springer-Verlag, Berlin, pp. 203-210.
Kiepenheuer, J., 1985, Can pigeons be fooled about the actual release site position by
presenting them information from another site?, Behav. EcoJ. SociobioJ. 183:75-82.
Kiepenheuer, J., 1986, Are site specific airborne stimuli relevant for pigeon navigation
only when matched by other release site information?, Naturwissenschaften 73:
42-43.
Kiepenheuer, J., Baldaccini, N. E., and Alleva, E., 1979, A comparison of orientational
and homing performances of homing pigeons of German and Italian stock raised
together in Germany and Italy, Monit. Zool. Hal. (N.S.) 13:159-171.
Lutgens, F. K., and Tarbuck, E. J., 1982, The Atmosphere: An Introduction to Meteorology,
2nd ed., Prentice-Hall, Englewood Cliffs, New Jersey.
Macadar, A. W., Rausch, L. J., Wenzel, B. M., and Hutchison, 1. V., 1980, Electrophys-
iology of the olfactory pathway in the pigeon, J. Compo Physiol. 137:39-46.
Michelsen, W. J., 1959, Procedure for studying olfactory discrimination in pigeons, Sci-
ence 130:630-631.
Miller, 1. H., 1941, Some tagging experiments with black-footed albatrosses, Condor 44:
3-9.
Murphy, R C., 1936, Oceanic birds of South America, Vols. I and II, American Museum
of Natural History, New York.
Neuhaus, W., 1963, On the olfactory sense of birds, in: Olfaction and Taste, Vol. 1
(Y. Zotterman, ed.), Macmillan, New York, pp. 111-123.
Ottar, B., Dovland, H., and Semb, A., 1984, Long range transport of air pollutants and
acid precipitation, in: Air Pollution and Plant Life (M. Treshow, cd.), Wiley, New
York, pp. 39-71.
Owen, R, 1872, On Dinornis (part XVI). Trans. ZooJ. Zoc. Lond. 7:381-396.
Owre, O. T., and Northington, P.O., 1961, Indication of the sense of smell in the Turkey
Vulture, Cathartes aura (Linnaeus), from feeding tests, Am. Mid. Nat. 66:200-205.
Papi, F., 1976, The olfactory navigation system of the pigeon, Verh. Dtsch. ZooJ. Gus. 69:
184-205.
Papi, F., 1982a, The homing mechanism of pigeons, Nature (Land.) 300:293-294.
Papi, F., 1982b, Olfaction and homing in pigeons: Ten years of experiments, in: Avian
Papi, F., 1986, Pigeon navigation: Solved problems and open questions, Monit. Zool. Ital.
(N.S.) 20:471-517.
Papi, F., Fiore, L., Fiaschi, V., and Benvenuti, S., 1971, The influence of olfactory nerve
section on the homing capacity of carrier pigeons, Monit. Zool. Ital. (N.S.) 5:265-267.
Papi, F., Fiore, L., Fiaschi, V., and Benvenuti, S., 1972, Olfaction and homing in pigeons,
Monit. Zool. Ital. (N.S.) 6:85-95.
Papi, F., Fiaschi, V., Benvenuti, S., and Baldaccini, N. W., 1973, Pigeon homing: Outward
journey detours influence the initial orientation, Monit. Zool. Ital. (N.S.) 7:129-133.
Papi, F., loale, P., Fiaschi, V., Benvenuti, S., and Baldaccini, N. E., 1974, Olfactory
navigation of pigeons: The effect of treatment with odorous air currents, J. Compo
Physiol. 94:187-193.
Papi, F., Keeton, W. T., Brown, A. 1., and Benvenuti, S., 1978a, Do American and Italian
pigeons rely on different homing mechanisms?, J. Compo Physiol. 128:303-317.
Papi, F., loale, P., Fiaschi, V. Benvenuti, S., and Baldaccini, N. E., 1978b, Pigeon homing:
Cues detected during the outward journey influence initial orientation, in: Animal
Migration, Navigation, and Horning (K. Schmidt-Koenig and W. T. Keeton, eds.),
Springer-Verlag, Berlin, pp. 65-77.
Parker, T. J., 1891, Observations on the anatomy and development of Apteryx, Philos.
Trans. R. Soc. 1828:25-134.
Parliment, T. H., and Croteau, R., 1986, Biogeneration of Aromas, American Chemical
Society, Washington, D. C.
Pasquill, F., 1974, Atmospheric Diffusion, Wiley, New York.
Phillips, J. B., and Waldvogel, J. A., 1982, Reflected light cues generate the short-term
deflector loft effect, in: Avian Navigation (F. Papi and H. G. Wallraff, eds.), Springer-
Verlag, Berlin, pp. 190-202.
Phillips, J. B., and Waldvogel, J. A., 1988, Celestial polarized light patterns as a calibration
reference for the sun-compass of homing pigeons, J. Theor. BioI., 131:55-67.
Quay, W. B., 1967, Comparative survey of the anal glands of birds, Auk 84:379-389.
Rasmussen, R. A., 1972, What do the hydrocarbons from trees contribute to air pollution?,
J. Air Poll. Contr. Assoc., 22:537-543.
Rice, H., Nochumson, D. H., and Hidy, G. M., 1981, Contribution of anthropogenic and
natural sources to atmospheric sulfur in parts of the United States, Atmos. Environ.
15:1-9.
Schmidt-Koenig, K., 1987, Bird navigation: Has olfactory orientation solved the problem?,
Q. Rev. Bioi. 62:31-47.
Schmidt-Koenig, K., and Phillips, J. B., 1978, Local anesthesia of the olfactory membrane
and homing in pigeons, in: Animal Migration, Navigation, and Horning (K. Schmidt-
Koenig and W. T. Keeton, eds.), Springer-Verlag, Berlin, pp. 119-124.
Schone, H., 1984, Spatial Orientation, Princeton University Press, Princeton.
Shallenberger, R., 1973, Breeding biology, homing behavior, and communication patterns
of the Wedge-tailed Shearwater, Puffinus pacificus, doctoral thesis, University of
California, Los Angeles.
Shallenberger, R. J., 1975, Olfactory use in the Wedge-tailed Shearwater (Puffinus pa-
cificus) on Manana Island, Hawaii, in: Olfaction and Taste, Vol. 5 (D. A. Denton and
J. P. Coghlan, eds.), Academic, New York, pp. 355-359.
Shumake, S. A., Smith, J. C., and Tucker, D., 1969, Olfactory intensity-difference thresh-
olds in the pigeon, J. Compo Physiol. Psychol. 67:64-69.
Simpson, J. E., Mansfield, D. A., and Milford. J. R., 1977, Inland penetration of sea-breeze
fronts, Q. f. R. Met. Soc. 103:47-76.
Smith, F. B., and Hunt, R. D., 1978, Meteorological aspects of the transport of pollution
over long distances, Atmos. Environ. 12:461-477.
Smith, S. A., and Paselk, R. A., 1986, Olfactory sensitivity of the Turkey Vulture (Cathartes
aura) to three carrion-associated odorants, Auk 103:586-592.
Snow, D. W., 1961, The natural history of the Oilbird, Steatornis caripensis, in Trinidad,
W. I., Zoologica (NY) 46:27-48.
Snyder, G. K., and Peterson, T. T., 1979, Olfactory sensitivity in the black-billed magpie
and in the pigeon, Camp. Biochem. Physiol. 62:921-925.
Snyder, R. L., and Cheney, C. D., 1975, Homing performance of anosmic pigeons, Bull.
Psychonom. Soc. 6:592-594.
Stager, K. E., 1964, The role of olfaction in food location by the Turkey Vulture (Cathartes
aura), LA Co. Mus. Contrib. Sci. 81:1-63.
Stager, K. E., 1967, Avian olfaction, Am. Zool. 7:415-420.
Stattleman, A. J., Talbot, R. B., and Coulter, D. B., 1975, Olfactory thresholds of pigeons
(Columba liva), quail (Colin us virginianus) and chickens (Gallus gallus), Camp.
Biochem. Physiol. 50A:807-809.
Stoddart, D. M., 1980, The Ecology of Vertebrate Olfaction, Chapman and Hall, London.
Stone, H., 1963, Determination of odor difference limens for three compounds, J. Exp.
Psychol. 66:466-473.
Strong, R. M., 1911, On the olfactory organs and sense of smell in birds, J. Morphol. 22:
619-662.
Sutton, O. G., 1947, The problem of diffusion in the lower atmosphere, Q. J. R. Met. Soc.
73:257-281.
Sutton, O. G., 1953, Micrometeorology, McGraw-Hili, New York.
Teichman, H., 1959, Concerning the power of the olfactory sense of the eel Anguilla
anguilla (L.), Z. Vergleichende Physiol. 42:206-254.
Tolhurst, B. E., and Vince, M. A., 1976, Sensitivity to odours in the embryo of the domestic
fowl, Anim. Behav. 24:772-779.
Waldvogel, J. A., 1987, Olfactory navigation in homing pigeons: Are the current models
atmospherically realistic?, Auk 104:369-379.
Waldvogel, J. A., and Phillips, J. B., 1982, New experiments involving permanent-resident
deflector loft birds, in: Avian Navigation (F. Papi and H. G. Wallraff, eds.), Springer-
Verlag, Berlin, pp. 179-189.
Waldvogel, J. A., Benvenuti, S., Keeton, W. T., and Papi, F., 1978, Homing pigeons
orientation influenced by deflected winds at home loft, J. Camp. Physiol. 128:297-301.
Waldvogel, J. A., Phillips, J. B., McCorkle, D. R., and Keeton, W. T., 1980, Short-term
residence in deflector lofts alters initial orientation of homing pigeons, Behav. Ecol.
Waldvogel, J. A., Phillips, J. B., and Brown, A.I., 1988, Changes in the short-term deflector
loft effect are linked to the sun compass of homing pigeons, Anim. Behav. 36:
150-158.
Walker, J. c., Walker, D. B., Tambiah, C. R., and Gilmore, K. S., 1986, Olfactory and
nonolfactory odor detection in pigeons: Elucidation by a cardiac acceleration par-
adigm, Physiol. Behav. 38:575-580.
Wallraff, H. G., 1979a, Goal-oriented and compass-oriented movements of displaced
homing pigeons after confinement in differentially shielded aviaries, Behav. Ecol.
Wallraff, H. G., 1979b, Olfaction and homing in pigeons: A problem of navigation or of

motivation?, Naturwissenschaften 66:269-270.
Wallraff, H. G., 1980a, Does pigeon homing depend on stimuli perceived during displace-
ment? I and II, ,. Compo Physio1. 139:193-208.
Wallraff, H. G., 1980b, Olfaction and homing in pigeons: nerve-section experiments,
critique, hypotheses, J. Compo Physio1. 139:209-224.
Wallraff, H. G., 1981, The olfactory component of pigeon navigation: Steps of analysis,
J. Compo Physiol. 143:411-422.
Wallraff, H. G., 1982, The homing mechanism of pigeons, Nature (Lond.) 300:293.
Wallraff, H. G., 1984, Migration and navigation in birds: A present-state survey with
some digressions to related fish behaviour, in: Mechanisms of Migration in Fishes
(J. D. McCleave, G. P. Arnold, J. J. Dodson, and W. H. Neill, eds.), Plenum, New
York, pp. 509-544.
Wallraff, H. G., and Foa, A., 1981, Pigeon navigation: Charcoal filter removes relevant
information from environmental air, Behav. Eco1. Sociobio1. 9:67-77.
Wallraff, H. G., and Hund, K., 1982, Homing experiments with starlings (Sturnus vulgaris)
subjected to olfactory nerve section, in: Avian Navigation (F. Papi and H. G. Wallraff,
eds.), Springer-Verlag, Berlin, pp. 313-318.
Wallraff, H. G., Papi, F., loale, P., and Foa, A., 1981, On the spatial range of pigeon
navigation, Monit. Zoo 1. Ital. (N.S.) 15:155-161.
Walter, W. G., 1943, Some experiments on the sense of smell in birds, Arch. Neerl.
Physiol. 27:1-73.
Wenzel, B. M., 1967, Olfactory perception in birds, in: Olfaction and Taste, Vol. 2
(T. Hayashi, ed.), Pergamon, Oxford, pp. 203-217.
Wenzel, B. M., 1968, Olfactory prowess of the kiwi, Nature (Lond.) 220:1133-1134.
Wenzel, B. M., 1971, Olfactory sensation in the kiwi and other birds, Ann. NY Acad.
Sci. 188:183-193.
Wenzel, B. M., 1982, Functional status and credibility of avian olfaction, in: Avian
Wenzel, B. M., 1983, Chemical senses, in: Physiology and Behaviour of the Pigeon
(M. Abs, ed.), Academic, London, pp. 149-167.
Wenzel, B. M., 1985, The ecological and evolutionary challenges of procellariiform ol-
faction, in: Chemical Signals in Vertebrates, Vol. 4 (D. Duvall, D. Muller-Schwarze,
and R. M. Silverstein, eds.), Plenum, New York, pp. 357-368.
Wenzel, B. M., and Rausch, L. J., 1977, Does the olfactory system modulate affective
behavior in the pigeon?, Ann. NY Acad. Sci. 290:314-330.
Wenzel, B. M., and Sieck, M. H., 1972, Olfactory perception and bulbar electrical activity
in several avian species, Physio1. Behav. 9:287-294.
Wilson, E. 0., Bossert, W. H., and Regnier, F. E., 1969, A general method for estimating
threshold concentrations of odorant molecules, J. Insect Physio1. 15:597-610.
Wiltschko, R., and Wiltschko, W., 1987, Pigeon homing: Olfactory experiments with
inexperienced birds, Naturwissenschaften 74:94-95.
Wiltschko, W., Wiltschko, R., and Jahnel, M., 1987a, The orientation behaviour of anosmic
pigeons in Frankfurt a.M., Germany, Anim. Behav. 35:1324-1333.
Wiltschko, W., Wiltschko, R., and Walcott, C., 1987b, Pigeon homing: Different effects
of olfactory deprivation in different countries, Behav. Ecol. Sociobiol. 21:333-342.
Wiltschko, W., Wiltschko, R., Gruter, M., and Kowalski, D., 1987c, Pigeon homing: Early
experience determines what factors are used for navigation, Naturwissenschaften

74:196-197.
Wright, R. H., 1958, The olfactory guidance of flying insects, Can. Entomal. 90:81-89.
Wright, R. H., 1964, The Science of Smell, Allen & Unwin, London.
Wilrdinger, 1., 1979, Olfaction and feeding behaviour in juvenile geese (Anser a. onser
and Anser domesticus), Z. Tierpsychal. 49:132-135.
INDEX
a-pinene, 279 Anser (cant.)

Accipiter, 133, 135 domesticus, 291
Accipiter nisus, 27 Anthus, 134
Acci pitridae, 65 Antilocapra americana, 253, 254
Acetate, 290 Apalis flavida, 165, 166
Acrocephalus Apalis, Yellow-breasted: see Apolis
arundinaceus, 158 flavida
palustris, 152, 154, 164 Aphelocoma coerulescens, 12
schoenobaenus, 153 Apodidae, 86
scirpaceus, 153, 154 Apteryx oustralis, 289, 290
Actitis macularia, 21, 38 Apus apus, 301
Adaptationist program, 51 Aquila chrysaetos, 201, 208, 209,
Aegypius monochus, 207 248-250
Africa, 143-169, 292 Arabia, 156, 157
African fauna, 146-152 Archilochus alexandri, 291
Agelaius phoeniceus, 4, 5, 55, 73, Ardea
82-86 cinerea, 67
Alaska, 156 herodias, 67
Alauda, 134 Ardeidae, 65, 67
Albany, 110, 111 Assortative mating, 68
Albatross, Black-footed: see Diomedea Astrapio
nigripes mayeri,78
Alcohol, 279 nigra, 78
Amazona ventralis, 245 rothschildi, 78
Amazona vittata, 245, 261 splendidissiana, 78
Amazonia, 164 stephaniae, 77
America, 145, 146 Atlantic Ocean, 124
American Ornithologists' Union, 233, Atlas Mountains, 148
240, 241, 258 Atmospheric structure, 109-131
Ammonium, 278-279 Australia, 86
Anas, 132, 134 Avoidance-image hypothesis,
platyrhynchos, 288 66, 67
Andes Mountains, 94 Aythyo, 132, 134
Animas Mountains, 254 americana, 28
Anser, 135 valisineria, 8, 18, 28, 29
anser, 291 Azores, 159
323
324 INDEX
Badger: see Mellivora capen sis California Polytechnic State University,

Bahamas, 86, 150 196
Bananaquit: see Coereba f/aveola Calliphora, 291
Bear Camaroptera simplex, 165
Black: see Ursus americanus Canis
Grizzly: see Ursus horribilis latrans, 204, 206, 210
Bee-eater: see Merops lupus, 253
Beetle, Red Flour: see Tribolium lupus baileyi, 254
castaneum Canvasback: see Aythya valisineria
Behavior, breeding, 289 Cape Province, 150
Benzaldehyde, 274, 275 Cape Saint Vincent, 155
Bishop, Red: see Euplectes orix Carbonyl, 279
Bison: see Bison bison Carduelis, 34
Bison bison, 254 carduelis, 61
Bitter Creek National Wildlife Refuge: see chloris, 61
Hudson Ranch f/ammea, 61
Black Sea, 157 tristis, 9, 61
Blackbird: see Icteridae, Turdus merula Carotenoid, 278
Brewer's: see Euphagus cyanocephalus Carpodacus
Red-winged: see Agelaius phoeniceus cassinii, 9, 61
Rusty: see Euphagus carolinus mexicanus, 61
Blackcap: see Sylvia atricapilla purpureus, 61
Bobcat: see Lynx rufus Carribean, 86
Bobolink: see Dolichonyx oryzivorus Carrizo Plain, 253, 254
Bobwhite, Northern: see Colinus Cascade Mountains, 159
virginianus Caspian Sea, 157
Bosphorus, 155 Castanea sativa, 159
Brachyramphus, 58 Cathartes aura, 205, 208, 237, 275, 276,
Brachystegia, 148 292
Brambling: see Fringilla montifringilla Central America, 144, 150
Branta, 135 Cercotrichas
Breckenridge Mountain, 225 galactotes, 165
Breeding grounds, fidelity to, 158 leucophrys, 165
Brood defense, 26, 30 Cerebral hemisphere, ipsilateral, 273
Brood reduction, 6 Cervus nann odes, 253
Bucephala, 132, 134 Ceryle rudis, 8
Budgerigar: see Melopsittacus undulatus Chaetodontidae, 86
Bullfinch, Eurasian: see Pyrrhula Chaffinch: see Fringilla coelebs
pyrrhula Charadrius, 134
Bunting, Indigo: see Passerina cyanea montanus, 253
Bunting, Snow: see Plectrophenax nivalis Chat, Rufous Bush: see Cercotrichas
Bureau of Land Management, 195, 254 galactotes
Burro: see Equus asinus Chen caerulescens, 23, 65, 66, 68
Butanethiol, 275, 276 Chickadee,
Butanol, 275 Black-capped: see Parus atricapillus
Buteo, 66, 133, 135 Carolina: see Parus carolinensis
jamaicensis, 225 Chicken, Domestic: see Gallus gallus
Chiffchaff: see Phylloscopus collybita
Caching, 290 Chromosomal hypothesis, 16, 17
Calidris, 134 Cicinnurus regius, 77
Caliente Mountains, 253 Circannual rhythms, 152
California, 175-263, 295 Circus, 135
California Department of Fish and Game, Citellus beecheyi, 183
184, 188, 195, 205, 210, 220-222, Clangula, 134, 135
233-237, 254 Climatic change, 144, 145
California Fish and Game Commission, Cloacal gland, 289
221, 222, 230, 239-242, 257 Cnemophilus macgregorii, 77
INDEX 325
Coccothraustes Crane
coccothraustes, 61 Mississippi Sandhill. see Grus
vespertinus, 61 conodensis pullo
Cod liver oil, 295, 296 Sandhill: see Gras canodensis
Coerebo j1aveola, 66 Whooping: see Gras omericono
Colinus virginianus, 8, 275, 276 Crossbill, Red: see Loxio curvirostro
Colombia, 150 Crotophytus wislizenii silus, 253
Color Cuba, 82
in communication, 51-97 Cuculidae, 65
conspicuous, 54 ff, 70--73 Cuyama Valley, 253
cryptic, 54 ff, 70-73 Cyonocitta stelleri, 61
dimorphism, 57-59, 65-68 Cyclohexane, 276
distincti ve, 54 ff Cygnus, 134, 135
hypothesis, 56, 57 olor, 7
in physiological functions, 69-70
polymorphism, 65-68 Dams, 188
seasonal changes, 54 ff Doption copense, 295
Colorado, 247 DDE,200
Coloration, 51-97 DDT, 189, 215
Coloration, flash, 73, 74 Deer, Mule: see Odocoilcus hemionus
Colorfulness, 51-97 Deflector lofts, 305-308
Columba, 132, 134 Delichon
livia, 66, 270, 274-276, 301-304, 307, urbica,28
310 Dendroico
palumbo, 123 discolor, 24
Commissurotomy experiments, 307-310 fuliginoso, 61
Compass orientation, 271 petechia, 55
Condor, Andean: see Vultur gryphus Diffusion coefficient, 280-282
release to wild, 246-251 Dioch, Black-faced: see Queleo quelco
Condor, California: see Gymnogyps Diomedeo nigripes, 296
californianus Diphyllodes
captive breeding of, 175, 244-246 mognificus, 77
conservation of, 175-263 respublico, 78
egg collecting of, 178, 179 Dispersal, natal, 12, 13
formation of captive flock, 210-214 Diurnal feeding hypothesis, 129, 130
gene pool, 239-241 Dolichonyx oryzivoras, 28
habitat, 207-210, 246-251 Dove, Rock: see Columba livia
mortality of, 202-207, 214-216, 237, Dreponornis
238 olbertisi, 77
nesting success of, 182, 185, 186, 190, bruijinii, 78
193,197-202,229,230,236,237 Drosophil melanogoster, 90
population estimates of, 184, 189, 191, Dryocopus pileotus, 221
195,196,231,232 Dunnock: see Prunello moduloris
recovery plan for, 233
release to wild, 246-251 Eagle, Golden: see Aquilo chrysaetos
symbol of wilderness, 217-226 Egg
Condor Research Center, 195 production, 21, 22
Congo basin, 145, 148, 150 sex ratio of, 4
Corogyps otrotus, 237, 292 Eggshell thinning, 189, 200, 201
Corvus, 132, 134 Egret
corox, 201, 208, 211 Reddish: see Egretto rafescens
frugilegus, 5, 288 Snowy: see Egretto thula
Cougar: see Felis con color Egretto
Courtship, 26, 27 coeruleo, 67
Cowbird, Brown-headed: see rufescens, 67
Molothras oter sacro, 67
Coyote: see Conis lotrons thulo, 67
326 INDEX
Elk, Tule: see Cervus nannodes Fox (cont.)

Elkhorn Plain, 253 San Joaquin Kit: see Vulpes macratis
Emberizidae, 65 mutica
England, 153 France, 250
Epimachus Friends of the Earth, 234
fastuosus, 78 Fringilla, 132, 134
meyeri,77 co~ebs, 60,61,85, 123
Equador, 146 montifringilla, 61
Equus asinus, 252 Fringillidae, 147
Erithacus rubecula, 86, 161 Frugivores, 162, 163
Ethanethiol, 275, 276 Fulmar, Northern: see Fulmarus glacialis
Ethiopia, 148 Fulmarus glacialis, 296
Ethyl butyrate, 291
Euphagus Galapagos Islands, 14
caralinus, 82, 84 Gallus gallus, 274-276
cyanocephalus, 84 Garrulus glandarius, 61
Euplectes Gasterasteus aculeatus, 65
axillaris, 9 Gaussian plume, 280, 281
orix, 9 Gavia, 135
pragne,84 Geographical barriers, 154-158
Eurasia, 159 Geospiza fortis, 14, 15
Eye color, 81 Geothlypis trichas, 82
Germany, 286, 303-311
Falco, 135 Gibralter, 155, 159
femoralis, 254 Glaciation, 144, 145
peregrinus, 221 Goldfinch
rusticolus, 72 American: see Carduelis tristis
Falcon European: see Carduelis carduelis
Aplomado: see Falco femoral is Goose, Snow: see Chen caerulescens
Peregrine: see Falco peregrinus Grackle, Common: see Quisculus
Falconidae, 65 quiscula
Fat, 119, 153, 154, 156, 157 Grand Canyon National Park, 252, 253
Fecundity, 23 Granivores, 162, 163
Felis concolor, 254 Greece, 156, 161
Ficedula Greenland, 155, 156
albicollis, 156 Grenada, 66
collaris, 81 Grosbeak, Black-headed: see Pheucticus
hypoleuca, 25, 76, 153, 156, 167 melanocephalus
Fighting-ability hypothesis, 92-94 Grouse, Red: see Lagopus lagopus
Finch Grus, 135
Cassin's: see Carpodacus cassinii americana, 245
Darwin's Medium Ground: see canadensis, 245, 253
Geospiza fortis canadensis pulla, 245
Gray-crowned Rosy: see Leucosticte Guinea savanna belt, 148, 151
atrata Gull
House: see Carpodacus mexicanus Glaucous-winged: see Larus
Purple: see Carpodacus purpureus glaucescens
Fledglings, 4 Western: see Larus occidentalis
Flight behavior, 121-126 Guppie: see Poecilia reticulata
Floaters, 10, 164 Gymnogyps californianus, 175-263
Florida, 148, 150, 237 Gyps fulvus, 207, 250, 251
Flycatcher Gyrfalcon: see Falco rusticolus
Collared: see Ficedula albicollis and
Ficedula collaris Haematopus palliatus, 18, 29, 30
Pied: see Ficedula hypoleuca Handicap principle, 90
Foraging, 162-166, 289-291, 293 Harderian gland, 289
Fox Hawfinch: see Coccothraustes
Gray: see Uracyon cinereoargentatus coccothraustes
INDEX 327
Hawk, Red-tailed: see Buteo jamaicensis Lagopus

Heat loss, convective, 118, 119 lagopus, 12
Heat loss, evaporative, 118, 119 mutus, 72
Heptane, 275, 276 Lake Chad, 157, 164
Heron Lake Charles, 110
Great Blue: see Ardea herodias Laniidae, 146
Grey: see Ardea cinerea Lanius, 162
Little Blue: see Egretta caerulea collurio, 155, 156
Reef: see Egretta sacra Larus
Heterogamy, 16, 17 occidentaJis, 296
Hexane, 274-276 glaucescens, 25
Hirundinidae, 146, 147 Leucosticte atrata, 9
Horning, 301-312 Lizard, Blunt-nosed Leopard: see
Honeyeater Crotophytus wislizenii silus
Cardinal: see Myzomela cardinaJis Loboparadisea sericea, 77
Orange-breasted: see Myzomela Lophorina superba, 77
jugularis Loria loriae, 77
Hopper Mountain National Wildlife Los Angeles Zoo, 175, 190, 206, 214, 223,
Refuge, 227 228,236,240,250,251
Hudson Ranch, 219, 243, 244, 253 Los Padres National Forest, 181, 183,
Humidity, fluctuations in relative, 116, 218, 227, 228
117 Louisiana, 110, 114
Hummingbird: see Apodidae Loxia curvirostra, 61
Black-chinned: see Archilochus Luscinia luscinia, 153
alexandri Lycocorax pyrrhopterus, 77
Hungary, 153 Lymantria dispar, 282
Lynx rufus, 200
Icteridae, 20
Icterus Macgregoria pulchra, 77
galbula, 78, 82, 89 Macrosmat, 278, 290
spurius,61 Magnetic compass, 297-301
!ctinia, 135 Magpie, Black-billed: see Pica pica
Incubation feeding, 26, 27 Mallard: see Anas platyrhynchos
Indian Ocean, 82, 158 Malurus
Indicatoridae, 292, 293 cyaneus, 8
Individual recognition hypothesis, 64 splendens, 8
Indomalaysia, 144 Manakin, 85
Insectivores, 162, 163 Manucodia
Iran, 157 ater, 77
Iraq, 157 chalybatus, 77
Isbelline: see Oenanthe isabellina comnii,77
Isoberlinia, 148 jobiensis, 77
Italy, 156, 159, 161, 303, 309-311 Martin
Ixoreus naevia, 61 House: see Delichon urbica
Purple: see Progne subis
Jaeger, Parasitic: see Stercorarius Sand: see Riparia riparia
parasitic us Mate
Jay protection, 27
Scrub: see Aphelocoma coerulescens quality, 92-94
Steller's: see Cyanocitta stelleri selection, 87-92
Junco, Dark-eyed: see Junco hyemalis Mating, assortative, 68
Junco hyemaJis, 13, 14, 61 Mediterranean, 148, 153-161, 167
Juniperus oxycedrus, 160 Mediterranean Sea, 157, 159
Juvenile sex ratio, 6, 7 Melanerpes erythrocephalus, 86
Melanism, 66
Kenya, 86, 146, 151, 162, 164 Melanitta, 134, 135
Kingfisher, Pied: see Ceryle rudis Mellivora capensis, 293
Kiwi, Brown: see Apteryx australis Melopsittacus undulatus, 118
328 INDEX
Melospiza melodia, 5, 9, 24, 61 Numenius, 134

Menthol, 275, 276 Nuthatch
Merops,8 Brown-headed: see Sitta pusilla
Methane, 278 Pygmy: see Sitta pygmaea
Mexico, 148, 150
Gulf of, 124, 127, 154
Microsmat, 278 Oceanites oceanic us, 295
Migration, 13, 109-135, 143-169 Oceanodroma
altitude of, 109, 120, 121, 124-128, 133 homochroa, 296
diel timing of, 117, 121-133 leucorhoa, 289. 294
evolution of, 143 If Odocoileus hemionus, 206
feeding during, 129, 130 Odor
step, 163, 164 convective mixing, 283-286, 293
Migratory behavior, 152-158 deprivation, 307-310
Migratory routes, 154-157 electroencephalographic response to,
Mimus polyglottos, 5, 8, 18, 26, 32, 33, 290
36, 39 inorganic, 277
Miombo, 151 mechanisms of dispersion, 280-287
Mockingbird, Northern: see Mimus organic, 277, 278
polyglottos plume, 282, 283, 288, 293, 296, 297
Molothrus ater, 9 respiratory response to, 290
Molt, 75, 152 transport, 277-287
Monogamy, 2 If Odors, as landmarks, 287-297
Monomorphism, 62-64 Oenanthe, 162
Mortality isabellina, 165
age-dependent, 14 oenanthe, 155, 165
juvenile, 11, 12 pileata, 165
patterns of, 10 pleschanka, 165
sex-dependent, 16, 17, 35, 36 Ohio, 286
Motacilla flava, 154, 156, 158, 167 Oilbird: see Steatornis caripensis
Motacillidae, 146 Olfactory
Moth, Gypsy: see Lymantria dispar bulb, 273, 274, 291, 293
Murrelet, Marbled: see Brachyramphus landmarks, downwind, 292-297
Musk, synthetic, 290 landmarks, short-range, 288-292
Myzomela mucosa, 306
cardinalis, 9 navigation, mosaic model of, 301
jugularis, 9 navigation, true, 301-313
ratio, 273, 293
sensitivity, 272
n-amyl acetate, 274, 275 threshold, 274-277
n-butyl acetate, 275 Olfactory orientation, 269-313
National Audubon Society, 178, 185, 188, atmospheric influences on, 277-287
189, 195, 222, 227, 232-234, 236, behavioral evidence for, 287-312
238-243, 257-260 chemical influence on, 277-287
National Geographic Society, 185 Ontario, 286
National Park Service, 252 Oriole, Northern: see Icterus galbula
Nature Conservancy, 252 Ovis canadensis, 253, 254
Navigation, true, 271, 272 Oxyura, 32, 143
Nearctic, 144, 145, 154 Oystercatcher, American: see
Nebraska, 247 Haematopus paIliatus
Neotropics, 148, 150, 158, 166, 167
Neotropic migrants, 147, 148
Nestlings, 4 Pachycephala, 82
New Mexico, 254 Pacific Ocean, 295
New York, 110 Pagodroma nivea, 294, 295
Nigeria, 158 Palaearctic, 143-169
North America, 71, 87, 148 Pandion, 135
INDEX 329
Paradigalla Photocensusing, 202, 235

brevicauda, 77 Phyllirea, 159
carunculata, 77 Phylloscopus
Paradisaea bonelli, 156
apoda, 77 collybita, 8, 161
decora,77 sibilatrix, 8, 155
guilielmi, 77 trochilus, 8, 156, 166
minor, 77 Pica pica, 37, 275, 276, 290
raggiana, 77 Picoides
rubra, 77 borealis, 6
rudulphi, 78 pubescens, 61
Paradisaeidae, 76, 77, 78 Pigeon, Wood: see Columba palumba
Paradise, Birds of: see Pareadisaeidae Piloting by landmarks, 271
Parental care, 4, 5 Pistacia, 159
Parental investment, 2-40 Plectrophenax nivalis, 26
female, 21-25 Pleistocene, 146
male, 25-27 Plover, Mountain: see Charadrius
Parotia montanus
carolae, 77 Plumage variability, 51-97
lawesii,77 Poecilia reticulata, 65
sefilata, 77 Poisoning, 179 ff
wahnesi,77 cyanide, 204, 206, 207, 215
Parrot lead, 179, 187, 194, 204-207, 242, 247,
Hispaniolan: see Amazona ventralis 248
Puerto Rican: see Amazona vittata strychnine, 179, 180, 187, 215
Thick-billed: see Rhynchopsitta Pollutants, 282-286
pachyrhyncha Polyandry, 37-39
Parulidae, 147 Polynesian Islands, 67
Parus Portugal, 153, 155
atricapillus, 61 Powerlines, 207, 246, 247
caeruleus, 23, 25 Predation, 70-73
carolinensis, 61 Predator-avoidence hypothesis, 129, 130
cristatus, 15 Procellariidae, 65, 289, 292, 294
major, 5, 7, 8, 12, 18, 30, 61, 64, 86, Progne subis, 64
291 Pronghorn: see Antilocapra americana
montanus, 15 Prunella modularis, 8, 39, 161
Passer domesticus, 9 Ptarmigan, Rock: see Lagopus mutus
Passerina cyanea, 76, 78 Pteridophora alberti, 77
Patuxent Wildlife Research Center, 245, Pterodroma cahow, 261
259 Ptilorus
Pentane, 274-276 magnificus, 78
Perfluoromonomethyl cyclohexane, 286 paradise us, 78
Pernis, 135 victoriae, 78
Peru, 237 Puerto Rico, 82
Petrel Puffinus
Bermuda: see Pterodroma cahow creatopus, 296
Cape: see Daption capense gravis, 295
Snow: see Pagodroma nivea griseus, 296
Petroica, 82 pacificus, 289, 294, 295
Phainopepla: see Phainopepla nitens puffinus, 294
Phainopepla nitens, 69, 70 Punjab, 158
Phalacrocorax aristotelis, 7 Pyridine, 290
Phalarope: see Phalaropus Pyrrhula pyrrhula, 161
Phalaropus, 58, 76
Pheromones, 280-282
Pheucticus melanocephalus, 76 Quelea quelea, 7, 9
Phoenicurus phoenicurus, 167 Quercus coccifera, 160
Phonygammus keraudenii, 77 Quisculus quiscula, 4
330 INDEX
Radar, 124, 133-135 Sexual selection, 58

Radiotelemetry, 134, 135, 176, 195, 202, agonistic, 83-87
204,205,207,234,236 epigamic, 83-87
Rainfall, 150-152 Shag: see Phalacrocorax aristotelis
Raptor Research Foundation, 241 Shearwater
Raven, Common: see Corvus corax Greater: see Puffinus gravis
Redhead: see Aythya americana Manx: see Puffinus puffinus
Redpoll: Common, see Carduelis Pink-footed: see Puffinus creatopus
flammea Sooty: see Puffin us griseus
Redstart: see Phoenicurus phoenicurus Wedge-tailed: see Puffin us pacificus
American: see Setophaga ruticilla Sheep, Bighorn: see Ovis canadensis
Resource use, 161-163 Shrike, Red-backed: see Lanius collurio
Rhamnus, 159 Siberia, 156, 157
Rhynchopsitta pachyrhyncha, 254 Sicily, 155
Rif Mountains, 148 Sierra Club, 234
Riparia riparia, 167 Sierra Madre Ridge, 226, 227
Robin Sierra Nevada Mountains, 159
European: see Erithacus rubecula Signals, 51-97
White-browed Scrub: see Cercotrichas Sisquoc Sanctuary, 193, 248, 249, 251,
leucophrys 253, 257
Rook: see Corvus frugilegus Sitta
Rosa, 159 pusilla, 8
Rostratula benghalensis, 58, 76 pygmaea, 8
Skua, South Polar: see Stercorarius
maccormicki
Snipe, Painted: see Rostratula
Sahara, 145, 148, 150, 153, 156-159, 163, benghalensis
167 Social ranking, 68
Sahel, 147, 148, 150 Somali, 147, 162
Salvadora persico, 148 Somateria, 134, 135
San Diego Zoo, 175,204,212,214, South America, 144, 146
221-223,236,246,251 Southeast Asia, 144
San Gabriel Mountains, 179 Sp~n, 152, 156, 159, 160, 161, 247
San Joaquin Valley, 191, 196, 209, 243, Sparrow
246, 250 Harris: see Zonotrichia querula
San Luis Obispo County, 196, 253 House: see Passer domestic us
Sandpiper, Spotted: see Actitis macularia Song: see Melospiza melodia
Santa Barbara County, 191, 193, 226, 227, White-crowned: see Zonotrichia
253 leucophrys
Sarcorhamphus papa, 292 White-throated: see Zonotrichia
Saxicola albicolis
rubetra, 158 Sparrowhawk, European: see Accipiter
torquata, 18, 31 nisus
Scandinavia, 123, 124 Species recognition
Sea breeze, odors in, 298-300 agonistic, 79-83
Seleucidis melanoleuca, 78 epigamic, 79-83
Semiopteri wallacei, 77 Squirrel, Beechey: see Citellus beecheyi
Senegal, 150, 151 Starling, European: see Sturn us vulgaris
Sensory cues, 53, 54 Status-signaling hypothesis, 59 ff
Serengeti, 151, 162, 163 Steatornis caripensis, 293
Sespe Sanctuary, 183-185, 188, 190-193, Stercorariidae, 65
197, 209, 215, 218, 219, 222-229, Stercorarius
236,243,248-251,257 maccormicki, 294, 295
Setophaga ruticilla, 78 parasiticus, 66, 68
Sex ratios, 2-40 Sterna hirundo, 27
Sex roles, 30-33, 71 Stickleback, Three-spined: see
Sexual dimorphism, 5, 14, 15, 58, 59 Gasterosteus aculeatus
Sexual imprinting, 80 Stone chat: see Saxicola torquata
INDEX :131
Storm-Petrel Uropygial gland, 288

Ashy: see Oceanodroma homochroa Ursus
Leach's: see Oceanodroma leucorhoa american us, 201
Wilson's: see Oceanites oceanicus horribilis, 179, 253, 254
Strigidae, 65 U.S. Fish and Wildlife Service, 178, 188,
Sturn us, 132, 134 190, 195, 227, 232, 234, 237~242,
vulgaris, 7, 8, 123, 291, 301 250, 257~260
Sudan, 150, 151, 153, 156 U.S. Forest Service, 181, 185, 188, 238,
Sulfur, 278, 279 257
Survival, female, 23, 24, 25
Swan, Mute: see Cygnus 0101'
Vanellus, 134
Sweden, 12
Vegetation belts, 150
Swift, Common: see Apus apus
Ventura County, 191, 227
Sylvia, 152
Viburnum, 159
atricapilla, 152, 155, 161
Vireo olivaceus, 37
borin, 152, 153
Vireo, Red-eyed: see Vireo olivaceus
communis, 156
Vireonidae, 147
curruca, 155
Vulpes macrotis mutica, 253
nisoria, 165
Vultur gryphus, 200, 205, 221, 2:l5~237,
Sylviidae, 146, 147, 164, 167
245, 250, 251, 258
Vulture
Temperature, 116, 117 Black: see Coragyps atratus
core, 118 Cinereous: see Aegypius monachus
Tern, Common: see Sterna hirundo European Griffon: see Gyps fulvus
Terpenes, 278, 279 King: see Sarcorhamphus papo
Territorial defense, 18, 19, 86 Turkey: see Cathartes oura
Thermal cell, 111~114
Thermal convection, 111 ~ 115
Wagtail, Yellow: see Motacilla fluva
Threat hypothesis, 59~64
Warbler
Thrush
Barred: see Sylvia nisorio
Nightingale: see Luscinio luscinia
Bonelli: see Phylloscopus bonelli
Varied: see Ixoreus naevio
Garden: see Sy lvio borin
Tibet, 158
Great Reed: see Acrocephalus
Tit
arundinaceus
Blue: see Parus caeruleus
Grey Wren: see Camaroptera simplex
Crested: see Parus cristatus
Marsh: see Acrocepholus palustris
Great: see Parus major
Prairie: see Dendroica discolor
Willow: see Parus montclIlus
Reed: see Acrocephalus scirpoceus
Tower kills, 124, 133
Sedge: see Acrocepholus
Tribolium castaneum, 88
schoenobaenus
Trimethylamine, 275
Yellow: see Dendroico petechiu
Trimethylpentane, 290
Willow: see Phylloscopus trochilus
Tringa, 134
Wood: see Phylloscopus sibilatrix
Tropic of Cancer, 154
Water loss, 118
Tsavo, 147, 163~165
Waves
Tsavo National Park, 151, 162
buoyancy, 114
Tunisia, 158
internal gravity, 114
Turbulence, Ill, 115, 119, 120, 127, 283
Weight loss, 22
Turdidae, 146, 161, 164, 167
West Indies, 66
Turdus, 134
Western Foundation of Vertebrate
merula, 12, 161
Zoology, 181
Tyrannidae, 147
Wheatear: see Oenanthe oenonthe
Capped: see Oenanthe pileata
Uganda, 146 Pied: see Oenanthe pleschanko
United States, 70, 127, 301, 303~311 Whitethroat, Lesser: see Sylvia curruca
University of California, Berkeley, 178 Widow, Red-shouldered: see Euplectes
Urocyon cinereoargentatus, 206 axillaris
332 INDEX
Widowbird, Long-tailed: see Euplectes Wren (cont.)

progne Superb Blue: see Malurus cyaneus
Winchat: see Saxicola rubetra Wytham Woods, 12
Wind
horizontal, 114, 115, 282-287 Xiphoplorus, 68
speed, 119, 120, 286-287 Xylocaine, 309
vertical, 111-114, 282-287
Wintering grounds, 159-166 Yellowstone National Park, 252
Wolf: see Canis lupus Yellowthroat, Common: see Geothlypis
Mexican: see Canis lupus baileyi trichas
Woodpecker
Downy: see Picoides pubescens Zaire, 146, 150, 156, 158
Pileated: see Dryocopus pileatus Zimbabwe, 150
Red-cockaded: see Picoides borealis Zonotrichia
Red-headed: see Melanerpes albicolis, 67, 68
erythrocephalus lateralis, 61
Wren leucophrys, 13, 60, 85
Splendid: see Malurus splendens querula, 55, 60, 61, 85

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CURRENT

George F. Barrowclough, American Museum of Natural History,

Springer Science+ Business Media, LLC

ISBN 978-1-4757-9920-0 ISBN 978-1-4757-9918-7 (eBook)

© 1989 Springer Science+Business Media New York

N o part of this book may be reproduced, stored i n a retrieval system, or transmitted

RANDALL BREITWISCH, Department of Biology, University of Miami,

GREGORY S. BUTCHER, Department of Zoology and Burke Museum,

GABOR 1. LOVEI, Laboratory of Functional Ecology, Department of

FRANK R. MOORE, Department of Biological Sciences, University of

SIEVERT ROHWER, Department of Zoology and Burke Museum, Uni-

NOEL F. R. SNYDER, Portal, Arizona 85632

HELEN A. SNYDER, Portal, Arizona 85632

JERRY A. WALDVOGEL, Section of Neurobiology and Behavior, Cor-

influences, such as predation and competition. Gabor Lovei of Hungary

MORTALITY PATTERNS, SEX RATIOS, AND PARENTAL INVESTMENT IN

5.2. Why Aren't More Birds Polyandrous? ...................... 37

THE EVOLUTION OF CONSPICUOUS AND DISTINCTIVE COLORATION FOR

GREGORY S. BUTCHER AND SIEVERT ROHWER

ATMOSPHERIC STRUCTURE AND AVIAN MIGRATION

PAUL KERLINGER AND FRANK R. MOORE

1. Introduction ......................................................... 109

3. Predictions .......................................................... 117

P ASSERINE MIGRATION BETWEEN THE P ALAEARCTIC AND AFRICA

1. Introduction ......................................................... 143

BIOLOGY AND CONSERVATION OF THE CALIFORNIA CONDOR

NOEL F. R. SNYDER AND HELEN A. SNYDER

1. Introduction ......................................................... 175

2.1. The Pre-Koford Era ............................................ 178

OLFACTORY ORIENTATION BY BIRDS

1. Introduction ......................................................... 269

INDEX .................................................................... 323

MORTALITY PATTERNS, SEX

The females of some birds appear to die

A subject of great interest to students of animal mating systems over

RANDALL BREITWISCH • Department of Biology, University of Miami, Coral Gables,

diversity of mating systems. Parental investment (PI) is defined as "any

Unbalanced sex ratios in populations of adult birds were once

2.1. Sex Ratios in Eggs

2.2. Sex Ratios in Nestlings and Fledglings

in either the primary or secondary sex ratios in Red-winged Blackbirds

2.3. Sex Ratios in Juveniles

of relatively high female PI or disparate adult mortality of the sexes

2.4. Sex Ratios in Adults

nature of male-biased adult sex ratios in birds by the taxonomic di-

We should expect to observe different mortality schedules for the

tribute to differential mortality between the sexes. These four differ-

3.1. Juvenile Mortality

include weaponry used by males in intra sexual competition for mates

3.1.1. Natal Dispersal and Mortality

If females suffer a cost in farther natal dispersal, there should be

3.1.2. Migration and Mortality

than males. In wintering White-crowned Sparrows, the sex ratio in a

3.2. Age-Independent Mortality

3.2.2. Heterogamy and Mortality

for rejection of the chromosomal hypothesis (see Myers, 1978). Heter-

assumption, especially for passerines (e.g., Ricklefs, 1977; Walsberg,

4. MALE AND FEMALE PARENTAL INVESTMENT

One might expect that, 15 years after Trivers's provocative paper,

4.1. The Problem of Currency

data to support a general assumption that females in monogamous spe-

4.2. Female Parental Investment

4.2.1. Egg Production