Seeking to Understand the Living Bird: The 1997 Margaret Morse Nice Lecture

17 Pages·1998·8.7 MB·English

by  Nicholas E Collias

2
Wilson Bulletin, 110(1), 1998, pp. 28-44
SEEKING TO UNDERSTAND THE LIVING BI1RD
The 1997 Margaret Morse Nice Lecture
NICHOLAS E. COLLIAS1 AND ELSIE C. COLLIAS
For over 50 years the classic study by Mar- bird, an impression still fresh after three-quar-
garet Morse Nice on the life and behavior of ters of a century. I was not then aware that
the Song Sparrow (Melospiza melodia) has anyone in my world had any real interest in
given a basic orientation and ideas for re- birds aside from myself and Peter Rabbit, the
search to investigators of the natural behavior hero of the bedtime stories by Thornton W.
of birds. She made the first detailed, long-term Burgess. It was far from my thoughts that any-
study of the behavior of wild birds color- one could make a living watching birds, until
banded for individual identification (Nice years later when a scholarship to the Univer-
1933, 1934). She had an excellent education sity of Chicago made possible for me a career
and the two volumes of her monograph on the in zoology and ornithology.
Song Sparrow (Nice 1937, 1943), one on pop- The situation was different for Elsie, some
ulations, one on behavior, are written from the of whose ancestors, like those of Margaret
viewpoint of basic biological problems, enliv- Nice, arrived in New England in the 1600s.
ened by her profound curiosity about the life Eventually, Elsie’s family settled in Tiffin,
of birds. Mrs. Nice was a firm believer in con- Ohio, near the Sandusky River. Her parents
firming for herself any important published encouraged her early interests in nature and
fact about bird behavior, which is the reason taught her the local birds. Her father. Heath
why research was a passion with her (Nice K. Cole, was a lawyer with a strong interest
1979). In this spirit of direct scientific inquiry, in the natural sciences. Elsie, before she start-
we wish to present some highlights of our ed school, developed a great interest in insect
own research. life, and readily prevailed on her father to
We have spent much of our lives trying to make her an insect net. She eventually donat-
understand the biology of avian behavior, es- ed a substantial insect collection to Heidelberg
pecially the function, causes, ontogeny and College, her alma mater in Tiffin. After a year
evolution of social behavior at the physiolog- in research on malarial mosquitoes with the
ical, individual and population levels of or- United States Public Health Service, Elsie
ganization (N. Collias 1991). The first part of went back to finish her Ph.D. work in zoology
this presentation will be given by Nicholas, at the University of Wisconsin, where we met.
the second by Elsie, but we have generally Our friendship included getting up well before
worked together. dawn to watch the prairie-chickens dance near
Let me briefly introduce ourselves. My ear- Plainfield, Wisconsin, where we were two of
ly childhood was in Chicago Heights, then a the thousands of guests that Fran and Fred
small town, where my family lived on the Hamerstrom introduced to these fascinating
edge of town. Soon after learning to read, I birds over the years. After Elsie and I were
discovered in the local library “The Burgess married we did our research together on birds.
Bird Book for Children” (Burgess 1919) with
UNIVERSITY OF CHICAGO
(1937-1942).
its magnificent color plates by Louis Agassiz HORMONES AND BEHAVIOR
Fuertes. These plates gave me names for the
common birds that I encountered in the nearby Mrs. Nice and her family moved to Chicago
fields and woods. I vividly recall my first in 1936 and bought a house near the Univer-
glimpse of a bluebird in an orchard. It seemed sity of Chicago where I was a student, and we
as if a fragment of the blue sky had fallen and became friends.
My
was flying about on the back and wings of a research career began after graduation
in 1937 when Professor W. C. Allee of the
University of Chicago zoology department
CA1 U9n0i0v9.5-of16C0a6li.fornia. Dept, of Biology, Los Angeles, hired me as his research assistant to work on
2 Corresponding author. the effects of hormones on the peck order of
28
Collias ami ColIlas • THE LIVING BIRD 29
SYNCHRONY GONADOTROPHIN« SEXUALBEHAVIOR general way with more current evidence as
OFINTERNAL V f
CYCLESWITH GONADS critically reviewed in 1996 by Buntin, who
ENVIRONMENT / also brings out the variation between different
PROLACTIN „ » PARENTALBEHAVIOR species of birds.
There are two general phases in the breed-
FIG. 1. Interactions between hormones and behav-
ior in the control of breeding behavior in doves and ing cycle of birds, a sexual phase stimulated
pigeons. Inhibition indicated by minus — sign. (After by pituitary gonadatrophin and gonadal ste-
( )
N. E. Collias 1952 and Collias and Collias 1984). roid hormones, and a parental phase dominat-
ed by pituitary prolactin. The gonadal hor-
mones stimulate pair formation, nest building
hens. Testosterone and estradiol had been iso- and copulation. Male Ring Doves stimulate
lated in pure form in 1935 (Marrian 1950). In the females to lay eggs, as I found in a con-
chickens, the cock’s testes secrete testoster- trolled experiment (N. Collias 1950), confirm-
one, the hen’s ovary secretes testosterone, es- ing Wallace Craig’s demonstration of the same
tradiol, and progesterone (reviewed in Collias thing in 1911. Gonadal hormones, together
and Collias 1984). with the mate, nest and eggs, also help bring
We found that ovariectomized hens injected about onset of incubation.
with testosterone became more aggressive and In 1935, Oscar Riddle and his colleagues
rose in the peck order, some from the bottom discovered that prolactin injected into laying
to the top (Allee et al. 1939). Ovariectomized hens stimulates maternal behavior, i.e., incu-
hens injected with the female sex hormone, bation and care of chicks. Sitting on eggs in
estradiol, became sexually receptive but they turn stimulates prolactin secretion. However,
did not rise in the peck order (Allee and Col- a hypophysectomized male pigeon that I in-
lias 1940). jected with estradiol thereupon paired with a
Rank in the peck order is decided by fight- normal female and helped her incubate her
ing or passive submission at the initial en- eggs for over a month, showing that prolactin
counter of each pair of birds. Success in initial is not absolutely necessary for parental be-
encounters between normal hens is correlated havior (N. Collias 1950), although it normally
with larger comb size, a specific indicator of stimulates it (Buntin 1996). By inhibiting go-
testosterone. In my Ph.D. thesis, using the nadotrophin, rising prolactin levels help end
path coefficient method of Professor Sewall the sexual phase of breeding.
Wright and with his advice, I found that a Today, comparative endocrinology of wild
much greater percentage of the variance in birds in nature is a relatively new and flour-
success was determined by differences in ishing field ofresearch, made possible by such
comb size than in body weight or in previous techniques as radioimmunoassay of minute
success, while molt had a depressing effect on hormone levels in the blood, a technique for
success (N. Collias 1943). which Rosalyn Yalow of New York received
Mrs. Nice, who was president of the Chi- a Nobel Prize in 1977. For many species of
cago Ornithological Society from 1939 to birds it has now been amply confirmed that a
1941, invited me to speak before that society, sexual phase dominated by steroid sexual hor-
and I spoke about hormones and behavior of mones is succeeded by a parental phase more
birds as a self-regulating system with positive or less dominated by prolactin (Buntin 1996),
and negative feedback relations. Ten years lat- for example, in the Song Sparrow (Wingfield
er (N. Collias 1950), I reviewed the literature and Goldsmith 1990).
on the subject in some detail.
UNIVERSITY OF WISCONSIN
Figure shows the interactions between the
1 (1947-1951). ANALYSIS OF FAMILY
environment, hormones, and behavior. Origi-
INTEGRATION AND VOCAL
nally it was based largely on pigeons and COMMUNICATION
doves (N. Collias 1952), but indications now
are that it may apply to many other birds as I served as Instructor in Zoology at the Uni-
well. This figure was confirmed by a review versity of Wisconsin for four years. After 3
of more recent literature in 1984 (Collias and and 1/2 years in the Army in World War II, I
Collias 1984), and I think is consistent in a was more interested in family life than in peck
—
30 THE WILSON BULLETIN • Vol. 110, No. 1, March 1998
orders. Like Mrs. Nice, who as a young girl (3-4 days) some specific individuals may lead
raised chickens, my first acquaintance with the other chicks to maternal clucking (from a
details of individual bird behavior was with speaker) or to a source of warmth (warm
chickens. The focus of my research at Wis- lamp) in a cool room. A chick that forges very
consin was on family integration, and this led far ahead of the others, however, may utter
to an interest in vocal communication—. distress cries and is likely to turn back to re-
Family integration and leadership. When join its companions. A good leader has both
a baby chick is lost, cold, hungry, thirsty, or independence, and empathy with companions
in pain, it utters distress cries (chirps). When or young ones (N. Collias 1952).
the chick is returned to its mother or to its Social guidance by the parent bird or other
siblings, or the specific distress is relieved, the individuals enters into every stage of social
chick promptly switches to pleasure notes development, and climaxes when birds learn
(twitters). To a newly hatched chick, the traditional migration routes from experienced
mother hen is a complex of warmth, physical individuals, as has been indicated for geese
contact, clucking sounds, and within about an and cranes (Lishman 1996). There has been a
hour, also a moving object. Loss of any one tremendous amount of work on social learning
of these maternal stimuli may cause the chick of the song of songbirds, including the Song
to give distress cries and when the stimulus is Sparrow (Hauser 1996, Kroodsma and Miller
restored it moves toward the source of the 1996), and this is related to species identifi-
stimulus, normally the mother hen (N. Collias cation.
1952). A basic code of vocal communication
.
In its social development the chick goes During World War II, The Bell Telephone
through a series of stages (N. Collias 1952, Company invented the sound spectrograph, a
1962): machine that makes precise visual pictures of
sounds and gives a harmonic analysis of
(1) Initial predisposition to response to cer-
sounds (Potter 1945). This machine has rev-
tain key stimuli.
olutionized the study of animal communica-
(2) Self-reinforcement of these responses
tion. Professor Martin Joos, a linguist at the
during an early sensitive period (filial
University of Wisconsin was one of the first
imprinting).
to obtain a sound spectrograph for scientific
(3) Increasing social discrimination and
recognition of individuals. studies. In 1953, he and I presented the first
spectrographic study of the repertoire of vocal
(4) Social independence, exploration and
signals of an animal, the domestic fowl (Col-
social maturity with age and experi-
lias and Joos 1953).
ence. Chicks on being isolated from
We
found that the spectrogram of chick
companions give progressively fewer
pleasure notes emphasizes ascending frequen-
distress cries as they get older.
cies, that of distress cries descending frequen-
The first two stages depend especially on cies. The two opposed vocal signals appar-
genetically determined predispositions, the ently express states of security and insecurity,
last two stages involve learning to a greater respectively. This is an example of what Dar-
extent. win (1872) called the principle of antithesis,
In 1935, Lorenz graphically described filial or that opposite states of mind as he put it,
imprinting of newly hatched Greylag Geese are accompanied by antithetical motor expres-
(Anser anser) that followed him about. In sions. The different vocal signals of chickens,
1950, I confirmed in a controlled experiment including those of their wild ancestor, the Red
that the day of hatching was a sensitive period Junglefowl (GalIus gallus) are composed of
in which chicks begin to follow the parent and elements that can be arranged in antithetical
that responsiveness fell off precipitously in pairs, in effect a code (N. Collias 1987):
succeeding days if first exposure to parental
stimuli is delayed (N. Collias 1952). (1) Pitch rises or falls.
Leadership among small chicks of a brood (2) Low versus high pitch.
may contribute to family integration. Among (3) Clear, distinct tones versus harsh
recently hatched chicks of about the same age sounds where harshness is defined
Collias and Collicis • THE LIVING BIRD 31
spectrographically as harmonic streaks
combined with a wide and superim-
posed spread of frequencies.
(4) Brief versus long notes.
(5) Soft (low amplitude) versus loud notes.
In different vocal signals, the first element
in pairs 2 to 5 above tends to attract chicks,
the second element usually repels them. Dif-
ferent combinations of elements produce dif-
ferent vocal signals. For example, soft, low-
pitched and brief notes as in clucking of a
mother hen attract baby chicks, as was con-
firmed by experiments with comparable arti-
ficial sounds (Collias and Joos 1953). But
harsh, loud, high-pitched and long sounds
strongly repel them and cause chicks to rush
to shelter. In the case of adults, loud, harsh FIG. 2. Self-reinforcement offilial following. Red-
head ducklings on day of hatching follow a person
and high-pitched sounds are also alarm cries, over standard course and distance better with each suc-
but harsh and lower-pitched sounds are cessive trial. Each dot is an average of 10 ducklings
threats. Quite similar elements in the vocal tested individually. (After Collias and Collias 1956).
signals of the Village Weaver Ploceus cucul-
(
latus), a passerine bird, indicate the generality
of the code (N. Collias 1963). thya americana ducklings, we confirmed that
)
The number of vocal signals or calls of the day of hatching is a sensitive period for
birds has often been underestimated. Mrs. imprinting as Fabricius (1951) had found for
Nice (1943) described 21 “chief vocaliza- other ducks. We also found that ducklings fol-
tions” for the Song Sparrow, in the pre-spec- lowed a substitute parent better and better as
trograph age. The Red Junglefowl has over 20 imprinting proceeded (Fig. 2); i.e., filial im-
distinct and readily recognizable vocal sig- printing is self-reinforced and a form of learn-
nals, supported by spectrographic analysis (N. ing defined as improvement of performance
Collias 1987), as does the Village Weaver with practice (Collias and Collias 1956). This
(Collias 1963 and unpubl. data). Not many means the day of hatching in ducks, as in
birds have been observed sufficiently to yield chickens, is a critical time during which
such an extensive repertoire of vocal signals mother and young gradually develop strong
(Kroodsma and Miller 1996). In species with social bonds to each other.
a graded and overlapping repertoire of vocal Observations on two species of ducks in na-
signals, quantitative analysis shows that dif- ture showed that the ducklings spend most or
ferent vocal signals can be readily recognized, all of the day of hatching in the nest with the
for example in the Brown Noddy, Anous sto- mother. Thus, after the first young hatched, a
lidus (Riska 1986). Blue-winged Teal Anas discors hen led her
( )
brood from the nest about 18 hours later, a
DELTA WATERFOWL RESEARCH
Canvasback Aythya valisineria hen only af-
STATION (1953-1955). FILIAL ( )
ter 24 hours in the nest (Collias and Collias
IMPRINTING OF WILD DUCKLINGS
1956).
On recommendation by Mrs. Nice to the For her graduate research at Clark Univer-
director, H. Albert Hochbaum, we were able sity, Mrs. Nice (1910) had counted various
to spend three summers at this research station natural foods eaten by a very tame Northern
at the south end of Lake Manitoba, Canada. Bobwhite (Colinus virginianus) that was im-
The station operated a large incubator in printed on her. Similarly, at Delta we imprint-
which eggs collected from nests of various ed several species of wild ducklings to our-
waterbirds in the wild were hatched and made selves as substitute parents so that we could
available to investigators. With Redhead (Ay- watch details of their feeding behavior as
32 THE WILSON BULLETIN • Vol. 110, No. 1, March 1998
closely as we wished without disturbing the shell of the nest and with special displays and
ducklings in the least. Different species of calls endeavors to attract an unmated female
ducklings placed together in the same white to enter his nest. If she accepts, she lines the
enamel pan. with various small aquatic inver- nest with fine grass tops and often also with
tebrates that we collected from the marsh, pre- feathers, mates with the male, incubates, and
ferred to feed on different species of inverte- does most or all of the work of feeding the
brates. For example, a Blue-winged Teal nestlings. The male builds more nests and
duckling placed in the pan along with small tries to attract more mates in this polygynous
snails and Daphnia ate the snails first, where- species. But if his nest is rejected repeatedly
as a Ruddy Duck (Oxyura jamaicensis) duck- by females, the male tears it down and weaves
ling ignored the snails and strained out all the a fresh nest in its place. He may have to build
Daphnia (Collias and Collias 1963). In theory, many nests for each one that fledges a brood.
such different feeding specializations illustrate Each brood leaves with the female.
the idea of the ecological niche and the prin- Evolution of weaving (Collias and Collias
—
ciple of competitive exclusion, whereby dif- 1964, 1984). Small body size and ability to
ferent species of animals can live together in construct a nest and place it in a wide range
a community (Hutchinson 1978). of nest sites may have been key factors in the
origin and evolution of passerine birds (Order
WEAVERBIRDS AND EVOLUTION OF
Passeriformes; N. Collias 1997). Like many
NEST-BUILDING BEHAVIOR
other tropical passerine birds, weavers build
(From 1956)
roofed nests (Collias and Collias 1964, 1984;
At the end of her autobiography (1979), N. Collias 1997). In Africa, we traveled about
Mrs. Nice expressed a long cherished wish to places Jim Chapin recommended, and we
that she could have gone to the arctic and to found as many nests of weavers as we could
the tropics. Modem travel facilities and great- (Collias and Collias 1964). We found that only
ly enhanced financial support for research the Ploceinae (true weavers) of the seven sub-
have now made such things possible for many families of Ploceidae (weavers) then recog-
of us. The National Science Foundation was nized by Chapin (1954) truly weaves the nest,
founded in 1950, and a few years later Elsie using interlocking loops of long green flexible
and I applied for a joint grant to go to Africa strips torn from the leaves of grasses or palms.
for a comparative study of nests and nesting Sibley and Monroe (1990) unite four of Chap-
behavior of weaverbirds. This was something in’s subfamilies into one that they call Plo-
that I had wanted to do ever since reading ceinae, but recognize much the same relation-
Alfred Emerson’s (1938) classic monograph ships. Weaving is a primary adaptation that
on termite nests as a study in the phylogeny enables safer placement of the nest which is
of behavior. To our surprise, we received the suspended from twigs or vines near the pe-
grant and my dream was about to be realized. riphery of trees, or the nest is slung between
Our friend, John Emlen, suggested we con- upright reed stems over water. The other sub-
tact James Chapin of the American Museum families recognized by Chapin thatch their
of Natural History, who was then residing nests of stiff, often dry grass stems or some-
with his wife Ruth, in central Africa at a Bel- times light twigs.
gian research station for tropical diseases. The Some of the true weavers add a long en-
Chapins were of inestimable help to us in trance tube about the bottom entrance of the
many ways. The Belgians also helped us nest that probably helps protect from snakes.
greatly. The director of the station even had a There is a convergent evolution of entrance
12-m observation tower built for us next to a tubes in African and Asiatic species of weav-
tree with a breeding colony of Village Weav- ers.
ers (Ploceus cucullatus). We caught many of In the lowland rain forest of eastern Zaire,
these birds in mist nets and were able to make I collected the nest of Malimbus ccissini, Cas-
one of the first studies in Africa of birds color- sin’s Malimbe, also now known as the Black-
banded as individuals (Collias and Collias throated Malimbe. This nest, with its very
1959). long, neatly woven entrance tube, is I think
The male Village Weaver weaves the outer the most finely constructed nest of any bird in
-
Collias and Collias • THE LIVING BIRD 33
the world. I knew of no specimen of this nest the thermal homeostasis in the nest of this
at that time in any American museum. species (see also White et al. 1975).
The genus Euplectes consists of true weav- The Sociable Weaver belongs to the sub-
ers which include a variety of bishop birds family Plocepasserinae (of Chapin 1954) as
and widowbirds. They have elaborate flight do the Grey-headed Social Weaver (Pseudoni
displays but their nests illustrate regressive grita arnaudi) and the White-browed Sparrow
evolution of weaving (Craig 1980). In South Weaver Plocepasseri mahali), both of which
(
Africa, we found a ground nest of the Long- we studied in Kenya (Collias and Collias
tailed Widowbird E progne)', this nest had 1978, 1980). The individual nests of the latter
(
.
only a very thin woven outer shell over a thick two species are often in physical contact, but
nonwoven lining of brown grasses. lack a communal roof, and their sleeping nests
Evolution of gregarious nesting by weav- have two entrance holes, an obvious defense
—
ers. Whereas forest-dwelling weavers are against nocturnal predators. In contrast to the
often solitary nesters, weavers of open coun- Sociable Weaver and the Grey-headed Social
try with an abundance of grass seeds and in- Weaver which may nest in large colonies and
sects frequently nest in a colony, often in iso- forage in large flocks well away from the nest
lated trees (Chapin 1954, Crook 1962). Other trees, the White-browed Sparrow Weaver
things that favor gregarious nesting include nests in small cooperatively breeding groups
feeding in large flocks well away from the and defends a small group territory within
nesting grounds, social guidance to good food which it feeds. The Plocepasserinae illustrate
sources, scarcity of trees for nests, and special the Friedmann (1935) principle of colonial
protection from enemies by cooperative de- breeding in species of birds whose nesting and
fense, or nesting in very thorny trees, or close feeding grounds are spatially separated,
to nests of stinging insects (reviewed by Col- whereas birds that feed in their reproductive
lias and Collias 1984; see also Siegel-Causey area are generally solitary or less gregarious
and Khartonov 1990). nesters.
Social stimulation may also play a role in Division of lab—or between male andfemale
gregarious nesting. In Senegal, we found that Village Weavers. The division of labor be-
colonies of Village Weavers with fewer than tween male and female birds in breeding be-
ten adult males attracted disproportionately havior can be measured in terms of metabolic
and significantly fewer females than did males demands of the acts involved (Orians 1961;
of larger colonies (Collias and Collias 1969). Collias and Collias 1967a, 1976; Paynter
This is an example of the F. Fraser Darling 1974). As a rough estimate of a very energy
(1938) principle of social stimulation to demanding act, flying by the Village Weaver
breeding. At UCLA, we found that moderate takes about six times the energy as just resting
crowding of Village Weavers in large aviaries under the same conditions. The male uses
stimulated renewed breeding and extended the much flying energy for building nests that are
breeding season (Victoria and Collias 1973). unsuccessful. Putting the total amount of fly-
Gregarious nesting culminates in the fa- ing to gather nest materials into energy terms,
mous apartment-style nest of the Sociable we estimated for the central African race P. c.
Weaver Philetairus socius of southwestern nigriceps that the male Village Weaver did 6-7
( )
Africa (Collias and Collias 1964, 1978; Mac- times as much work for nest building as did
lean 1973). The huge compound nest is the female who merely lines the nest. By the
thatched of straws with light twigs added to same criterion of amount of flying required,
the communally built roof that helps protect the female did about twice as much work in
the birds from some enemies, sun and weath- foraging for food for the nestlings as did the
er. The underside of a nest mass has numerous male. Details of the analysis are given else-
openings to the separate nest chambers. A col- where (Collias and Collias 1967a, 1984:183-
ony we saw in South Africa was said by local 187).
farmers to have occupied the same two trees The division of labor between male and fe-
for over 100 years. Our colleagues at UCLA, male varies in different subspecies of Village
Bartholomew, White, and Howell (1976) Weaver (Table 1; Collias and Collias 1967a,
found that the larger the nest mass, the greater 1970, 1971, 1984). In the west African race.
34 THE WILSON BULLETIN • Vol. 110 No. 1, March 1998
,
TABLE mate selection by the female Village Weaver
1. Nests, polygyny, and nestling care in
in large outdoor aviaries. Doctoral and post-
three races of Village Weaver, Ploceus cucullatus
doctoral students on this problem have includ-
Western Central Southern ed Janice Victoria McClean, Catherine H. Ja-
Africa Africa Africa
cucullatus nigriceps spilonotus cobs, Florence McAlary McFarland and Cath-
Aver. min. temp, when leen R. Cox.
breeding 24° C 1 1°C 14° C To attract an unmated female, each male of
Number of males 9 18 11 the colony hangs beneath the bottom entrance
Nests built in two weeks 3.3 1.4 1.9 to his nest flapping his wings vigorously and
Mates per male 3.1 1.8 2.0
Feeding rate per hour per nest: uttering cries distinctive of each individual. It
is a spectacular sight when all males of a col-
by male 0.1 2.3 1.4 A
by female 4.1 4.7 4.2 ony display and call simultaneously. visit-
number of nests 15 11 39 ing female inspects the nest interior and sig-
nifies her acceptance by lining the nest and
aAfterCollias and Collias 1984:55.
copulating with the male.
Janice (Victoria 1969) found that both a
the male scarcely feeds the nestlings and de- male and his nest are essential for a female to
votes his energy to building more nests and choose a mate and lay eggs. Cathy (Jacobs et
getting more mates, and he is more polygy- al. 1978) found that nests accepted by females
nous. The central African race was observed were displayed by the male more than twice
in a cool mountain habitat where the young as often on the day of acceptance as nests that
apparently need more food, and the male often were rejected. The male’s wing display reveals
helped the female feed the nestlings, leaving and is greatly enhanced by the bright yellow
him less time to build nests and get mates. wing linings, and if we painted the wings
The south African race is intermediate. black, such males attracted significantly fewer
It is desirable to measure actual energy ex- mates than did control males (E. Collias et al.
penditure directly in the field. During the last 1979). Very young adult males and very old
two decades (Carey 1996), measurement of males are also discriminated against by the fe-
field metabolic rates has proved feasible with males (N. Collias et al. 1986). A female may
the doubly-labled water technique, clearly de- change mates between broods, but she has a
scribed by Nagy (1989). This technique mea- significant tendency to select her previous
C0
sures production rate and therefore over- mate or a familiar territory for subsequent
2
all energy expenditure over a specific period broods (McAlary 1985).
of time. For example, Flint and Nagy (1984) A nest has to last at least a month from the
UCLA
of found that the metabolic rate during time the female accepts it until the young
flight of free-ranging Sooty Terns (Sternafus- fledge. As a nest ages, it turns brown. The
cata) was about five times the standard resting female prefers a fresh green nest, and she pre-
metabolic rate. fers a fresh nest painted green to a fresh nest
M—ate selection by thefemale Village Weav- painted brown (Jacobs et al. 1978), so color
er. Darwin’s (1871) theory of sexual selec- of the nest is one factor in her choice.
tion has attracted renewed attention in the last The strength of nest materials is very im-
two decades (Andersson 1994), but Darwin portant to the female’s choice. If a male’s nest
had little to say about the role of nest-building is repeatedly rejected, he tears it down and
behavior in courtship and mate selection. builds a fresh nest in its place, so fragmented
Long ago. Mrs. Nice (1943:179) pointed out materials from discarded old nests litter the
that for birds “Symbolic building is charac- ground. If the birds in an aviary are given no
teristic of courtship in many species.” The fresh nest materials, they will pick up and
male Village Weaver carries this process one build nests of the old fragmented materials. A
step further in that he weaves the complete male displays his most recently built nest the
outer shell of the nest that he then displays to most, and so may induce a female to tempo-
unmated females. rarily accept such a trash nest. But we and our
Over the years we and our associates at associates found that females laid eggs in sig-
UCLA did many controlled experiments on nificantly fewer trash nests than in still older
Collias and Collias • THE LIVING BIRD 35
brown nests built of normal materials (Collias TABLE 2. Principles of animal breeding in evo-
and Collias 1984).
lution theory."
In conclusion, the nest of the male Village
Animal breeding Evolution theory
Weaver, as well as the male himself, are both
important considerations in the female’s 1 . Partially inbred lines 1 . Random genetic drift
choice of a mate. in local populations
2. Mass selection 2. Selection between in-
RED JUNGLEFOWL BEHAVIOR AND dividuals and families
MECHANISMS OF EVOLUTION 3. Cross breeding and line 3. Differential emigration
(From 1960) breeding from local populations
Since my research career began with the aAfterSewall Wright.
analysis of behavior in domestic chickens,
and, yet with a basic drive as a naturalist, it
was understandable that I should be most cu- a phenomenon shown recently to occur fre-
rious as to the behavior in nature of the wild quently in color-banded populations of the
ancestor of the domestic fowl, i.e., the Red Song Sparrow on small islands off the coast
Junglefowl. During the academic year of of British Columbia (Smith et al. 1996).
1962-1963, with financial support from the Wright (1978b) states that he derived his
National Science Foundation and the Guggen- theory of the mechanisms of evolution from
heim Foundation, we were able to carry out a the principles and history of animal breeding
field study of this bird in nature (Collias and (Table 2). Evidence from the breeding of
Collias 1967b), with special reference to its chickens supports his theory (Collias and Col-
behavioral ecology and population breeding lias 1996). Many new breeds and varieties of
structure. We then tried to relate our results to chickens have been produced by a combina-
mechanisms of evolution. tion of cross breeding and line breeding. As
The principal theory relating genetics and the primary and perhaps sole ancestor of the
evolution is the theory of Sewall Wright much studied domestic fowl, the Red Jungle-
(1932, 1978a) that adaptative evolution de- fowl is eminently suited for a study of genetic
pends most importantly on the shifting bal- mechanisms in evolution.
ance between the factors of evolution acting After making a preliminary study of a free-
on a species that is subdivided into many par- ranging population of this species on the
tially isolated local populations. This theory is grounds of the San Diego Zoo, we visited
opposed to the idea that a species consists ba- southeast Asia, and then we went on to India
sically of a single randomly breeding popu- for a study of the bird during its breeding sea-
lation. son. Dr. Salim Ali of the Bombay Natural His-
The significant question here is the nature tory Society advised us that a good place to
of the breeding structure of populations in na- find Red Junglefowl was in the Saharanpur
ture. One of the first attempts to relate the forest district in the Himalayan foothills.
population structure of a wild bird species in There we received much help from the Wild-
nature to Wright’s theory was in 1947 when life Preservation Society of India. We ob-
Alden H. Miller plotted the population data of served the junglefowl from a platform in a
Mrs. Nice on the Song Sparrow to emphasize tree, from a car, through a telescope when they
very limited dispersal distance of juvenile came to drink at a waterhole, by following
birds from their birthplace to breeding place. them about from elephant back, and by cap-
Miller (1947:139) concluded that the Song turing them in nets and nooses with the assis-
Sparrow, an abundant and widespread species, tance of the local people. The appearance of
“actually is seen to exist in small effective chicks coincided with onset of the rains and
breeding units” subject to considerable ran- of flights of termites, an important food for
dom differentiation in accord with Wright’s the chicks, and this coincidence may help de-
theory. Wright (1940) considered especially termine the breeding season.
important for evolution the case where local We located roosts when the cocks crowed
populations are liable to frequent extinction at dawn. The roosts were located in or near
with restoration from a few stray immigrants, small branch ravines in western Thailand
—
36 THE WILSON BULLETIN • Vol. 110, No. 1, March 1998
(Collias and Saichuae 1967), and along larger populations is expected, aside from local dif-
water courses in India. When the birds were ferences in conditions of selection. In a recent
not disturbed they occupied the same roosts review of electrophoretic studies of allozyme
throughout the breeding season in India (Col- variation in wild populations of 63 species of
lias and Collias 1967b). birds, Stangel (1991) found that island popu-
There seemed to be little difference be- lations were significantly more differentiated
tween the behavior of Red Junglefowl in na- than mainland populations, and that differ-
ture and in the free-living population at the ences were significantly correlated with dis-
San Diego Zoo where the birds formed sepa- tance between sample localities.
rate populations in different ravines with very
little interchange between local populations The second part of this presentation of our
(Collias et al. 1966). We had color-banded research is given by Elsie, who describes
most of the junglefowl in the zoo, and now some aspects of the development of behavior
focused on one large ravine where over a 7- in birds, and also genetics of egg-color poly-
year period we were able to get the lifetime morphism as related to behavior.
breeding success of many of the birds, some-
thing that would have been very difficult in I am honored to be asked along with my
the field. We found that only a very small pro- husband to give the first Margaret Morse Nice
portion of the birds, including the most dom- lecture. I grew up in northern Ohio during the
inant cock and most dominant hens, produced period when Mrs. Nice did her classic field
most of the adults of succeeding generations study of the Song Sparrow in Columbus,
(Collias et al. 1994, Collias and Collias 1996). Ohio. However, I did not meet Mrs. Nice until
Of 8 successive males at the top of the peck after Nick and I were married.
order of cocks, one male (Male AA) had a As my husband mentioned we met at the
longer tenure and copulated more often than University of Wisconsin where I was finishing
the other 7 despots combined. He also mated my Ph.D. work. We were married the next
twice as often as his 19 subordinates put to- year. Ever since we have worked as a team on
gether. The three hens at the top the peck or- the behavior of birds, in this country and over-
der of hens added more offspring of breeding seas.
age to the population than did the remaining INHERITED AND LEARNED COLOR
25 adult hens of the flock for which we had
PREFERENCES
lifetime breeding success. These findings ac-
cord with the dynasty principle elucidated by Initial response to parental bill color by
Newton (1989) in his summary of long-term chicks of Franklin’s Gull (Larus pipixcan).
studies by various investigators of different While at the Delta Waterfowl Research Sta-
bird species in nature. When allowance was tion in 1955 we did an experiment on the ini-
made for differential production of progeny tial response of incubator-hatched Franklin’s
and isolation by distance, the genetically ef- Gull chicks to parental bill color (Collias and
fective breeding size of our Red Junglefowl Collias 1957).
population was estimated at only about 13% We presented two different bill colors si-
of the adult population (Collias and Collias multaneously to a Franklin's Gull chick on the
1996). day it hatched in order to test the very first
In conclusion, the behavior of the Red Jun- responses of the chick to parental bill color.
glefowl can be related to Wright’s shifting bal- The method used was to present to the chick
ance theory of evolution through the effect of a flat piece of immobile cardboard on which
behavior on the breeding structure of popu- two simple models of adult Franklin’s Gull
lations. Social behavior exerts a reciprocal ef- heads were facing each other. Each head had
fect on evolution by structuring the population a differently colored bill. The bills of the two
into traditional roosts and by greatly reducing heads were actually holes in the cardboard be-
the genetically effective breeding size of local hind which different colors could be placed
populations through competition among indi- on both sides. The impression of motion was
viduals and families. Therefore, considerable accomplished by having a light behind the
random differentiation in and among local heads flash on and off 85 times a minute.
—
Collins and Collins • THE LIVING BIRD 37
stimulating the chicks to respond to the mod-
els. The chicks were taken right from the in-
cubator and it was the first experience the
chicks had with any color or the opportunity
to peck at a bill or to even see a shape like
that of an adult gull’s head.
The colors tested were red, the color of an RING ROOF EGG CHAMBER
adult Franklin’s Gull bill, versus white, or red
versus green. The number of times a chick
pecked at each color was recorded. Seventeen
chicks each tested for six minutes, pecked the
red bill 15 times more often than they pecked
at the white bill and 4 times more often than
they pecked at the green bill. Both results
were statistically significant. We concluded
that newly hatched Franklin’s Gull chicks
have a genetically determined predisposition
FIG. 3. Sequence of stages followed by a male
to peck at a parental bill of the normal red Village Weaver in weaving his nest (Collias and Col-
We
color over white or green. believe this ex- lias 1962).
periment was the first confirmation with in-
cubator-hatched young and without the use of
one tube and finish that tube completely be-
hand-held models of the classic experiments
fore they had finished half of any other color.
by Tinbergen and Perdeck (1950) showing
This result shows a tendency to exploit a
that the feeding responses of newly hatched
known source of nectar before exploring an-
Herring Gull Larus argentatus) chicks are
(
other regardless of color.
stimulated by the sight of the red spot on the
In conclusion, Anna’s Hummingbirds can
lower mandible of the yellow bill of the par-
probably learn any flower color that indicates
ent.
Anna’s Hummingbirds (Calypte anna) a good nectar flow.
trained to select different colors infeeding. WEAVING OF THE NEST BY THE MALE
Since most of the things one can buy for feed- VILLAGE WEAVER
ing hummingbirds are red, I decided to test if As you know we studied weaverbirds, par-
hummers really had a preference for red. I ticularly the Village Weaver for many years,
tested red, blue, yellow and colorless solutions
of sugar water in various experiments (Collias and I am going to describe some phases of
and Collias 1968). our work. First, I want to describe how a
weaverbird makes a nest (Collias and Collias
I trained hummers to come to a given color
1962, 1984).
by presenting all four colors simultaneously, A
typical Village Weaverbird nest built by
but only the solution to which the humming
an experienced male adult weaver doesn’t
birds in our garden were being trained had
look much like a typical nest from North
sugar in it. All the other colors were just col-
America. It is roofed, has a bottom entrance,
ored water.
When testing, I presented the same colors and is woven of strips torn from the leaves of
grasses or palms.
as in the training period but this time all colors
Figure 3 shows the various stages in build-
were just water without sugar. In all cases the
ing of a Village Weaverbird nest. Each stage
bird visited the color to which it had been
of the nest provides the stimulus for the next
trained by far the most often. This result
stage.
showed a tendency to persist at a given color
that indicates a good source of nectar before (1) Only the male weaves a nest and he se-
shifting to another color. lects a site which is quite far out on a
When I tested all four colors in different small branch, and preferably at a fork. He
test tube feeders with the same concentration first builds a ring. Then while standing in
of sugar I found the hummers would start on the ring he builds the rest of the nest. He