Wilson Bulletin, 110(l), 1998, pp. 28-44

SEEKING TO UNDERSTAND THE LIVING The 1997 Margaret Morse Nice Lecture

NICHOLAS E. COLLIAS.2’ 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- 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 and . 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, Elsies’ 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. was flying about on the back and wings of a My research career began after graduation in 1937 when Professor W. C. Allee of the ’ ’ Univ. of California, Dept. of Biology, Los Angeles, University of Chicago zoology department CA 900951606. hired me as his research assistant to work on * Corresponding author. the effects of hormones on the peck order of

28 Collias and CoZZiasl THE LIVING BIRD 29

SYNCHRONY - GONADOTROPHIN - SEXUAL BEHAVIOR general way with more current evidence as OF INTERNAL 4 f CYCLES WITH critically reviewed in 1996 by Buntin, who ENVIRONMENT I-) I /G0NAGSi also brings out the variation between different PROLACTIN _ PARENTAL BEHAVIOR of birds. FIG. I. Interactions between hormones and behav- There are two general phases in the breed- 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 (Martian 1950). In the females to lay eggs, as I found in a con- chickens, the cocks’ testes secrete testoster- trolled experiment (N. Collias 1950), confirm- one, the hens’ ovary secretes testosterone, es- ing Wallace Craigs’ 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 of research, 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. Figure 1 shows the interactions between the UNIVERSITY OF WISCONSIN environment, hormones, and behavior. Origi- (1947-1951). ANALYSIS OF FAMILY nally it was based largely on pigeons and INTEGRATION AND VOCAL doves (N. Collias 1952), but indications now COMMUNICATION 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 l/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. IZO, No. I, 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 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 studies. In 1953, he and I presented the first recognition of individuals. 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 (Gallus 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 - .. - .. ______.___-____ LHb’ 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- s l pitched and brief notes as in clucking of a 8 20- mother hen attract baby chicks, as was con- a firmed by experiments with comparable arti- if ol...... ficial sounds (Collias and Joos 1953). But 10 20 30 harsh, loud, high-pitched and long sounds TRIALS strongly repel them and cause chicks to rush FIG. 2. Self-reinforcement of filial following. Red- to shelter. In the case of adults, loud, harsh 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 ( cucul- Zatus), a 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 (195 1) 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 Zidus (Riska 1986). Blue-winged Teal (Anus discors) hen led her brood from the nest about 18 hours later, a DELTA WATERFOWL RESEARCH Canvasback (Aythyu 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. IIO, No. I, Mm-ch 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 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 (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 tom 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 ins’ subfamilies into one that they call Plo- that I had wanted to do ever since reading ceinae, but recognize much the same relation- Alfred Emersons’ (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 cassini, Cas- one of the first studies in Africa of birds color- sins’ 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 Cdias and Cdias l 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 consists of true weav- The 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 labor between male and female 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 E 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 (Philetuirus 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. I, March I998

mate selection by the female Village Weaver TABLE 1. Nests, polygyny, and nestling care in three races of Village Weaver, Ploceus cucullatus.” in large outdoor aviaries. Doctoral and post- doctoral students on this problem have includ- WNUtl CeIltEd Southern Africa Africa Africa ed Janice Victoria McClean, Catherine H. Ja- cucullirtus ?ligiCepS’ spilonotus cobs, Florence McAlary McFarland and Cath- Aver. min. temp. when leen R. Cox. breeding 24” C 11°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 happing 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 by female 4.1 4.7 4.2 ony display and call simultaneously. A visit- number of nests 15 11 39 ing female inspects the nest interior and sig- nifies her acceptance by lining the nest and aAfter Collias and Collia~ 198455. 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 males’ 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 sures CO, production rate and therefore over- mate or a familiar territory for subsequent 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 of UCLA 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 catu) 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 Mate selection by the female Village Weav- painted brown (Jacobs et al. 1978), so color er.-Darwins’ (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 females’ choice. If a males’ 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 C&Zias and CoZZiasl 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 Weaver, as well as the male himself, are both Ammal breeding Evolution theory important considerations in the females’ 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 BAfter Sewall Wnght. 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 Wrights’ 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 Wrights’ 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 l Vol. 110, No. I, 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 25 adult hens of the flock for which we had INHERITED AND LEARNED COLOR lifetime breeding success. These findings ac- PREFERENCES cord with the dynasty principle elucidated by Initial response to parental bill color by Newton (1989) in his summary of long-term chicks of Franklins’ Gull (Lams 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 Franklins’ 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 Franklins’ 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 Wrights’ 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 Franklins’ 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, Collias and Collias * 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 gulls’ head. The colors tested were red, the color of an RING ROOF EGG CHAMBER adult Franklins’ 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 Franklins’ Gull chicks ANTECHAMBER ENTRANCE 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- color over white or green. We 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 urgent&us) chicks are other regardless of color. stimulated by the sight of the red spot on the In conclusion, Annas’ Hummingbirds can lower mandible of the yellow bill of the par- probably learn any flower color that indicates ent. a good nectar flow. Annas’ Hummingbirds (Calypte anna) trained to select difSerent colors in feeding.- 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 and I am going to describe some phases of of sugar water in various experiments (Collias our work. First, I want to describe how a and Collias 1968). 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 doesnt’ 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. and is woven of strips torn from the leaves of When testing, I presented the same colors 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 38 THE WILSON BULLETIN l Vol. 110, No. I, March 1998

always stands in the same place and al- adult (Collias and Collias 1964). So we de- ways faces in the same direction. cided to see what a bird had to develop or (2) He builds the roof over his head and in learn in order to build a typical nest. front of him pushing and building out A young Village Weaver that I raised from as far as he can, and so ends up build- before he had his eyes open we called Tex as ing the globular nest chamber. a shortened form of Textor which means (3) Then he builds over his head toward his weaver and which at that time was the generic back and forms the antechamber. When name of this group of weaverbirds. Little did he gets the antechamber down to the I realize at the time that Tex was only the first horizontal he neatly finishes off the en- of 41 weaverbirds I was going to hand rear. trance. Then he thatches a ceiling of rel- After Tex could feed himself we kept him atively short wide strips. in a cage that was large enough that we could (4) His standing in one place and pushing furnish him with giant reed grass (Arundo out in all directions determines the size donux) for nest materials, as we did the adults and shape of the nest. in the outdoor aviary. A nest built by Tex in (5) The threshold where he keeps his feet his second year was pretty good. At this point serves as a ridge to keep the eggs from he had neither seen nor even heard another rolling out of the bottom of the nest Village Weaver so neither tuition nor example chamber. is necessary for a male weaver to build a (6) After a female accepts a nest he adds a nest-then just what was necessary? short entrance tube 4-8 cm long. This I reared some male weavers in the complete is the only part of the nest he adds absence of any natural materials that could be while outside the nest, probably be- used for building. When these birds were sev- cause the female wont’ let the male en- en months old I tested their preference for dif- ter the nest after she accepts it. ferent colors with colored toothpicks which gave a standard size, shape and weight, rep- Figure 4 shows some of the motions a male resenting nest materials. During the first four goes through to push and pull a strip into his days of testing, preference of the young weav- ring. Note that if the strip is too long for him ers for green increased significantly (P = to push all of it through, he brings the loop 0.01) from 38% to 71%. around and weaves it in. He then takes the At first the males will try to weave with any loose end of the strip and weaves it in. strip even if it is much too short. By measur- After studying how a weaver makes his nest ing the length of all the strips in two nests of we attempted to weave a nest ourselves with the same bird, we found that a male Village forceps, using as near as possible the same Weaver in his first breeding season as an adult general techniques as the male, and we man- builds with strips that average twice as long aged to make a nest that was a reasonable fac- as those he used as a yearling. simile of a normal nest (illustrated in Collias The birds also have to learn the mechanics and Collias 1962). of weaving and where to weave. We found retarded development of weaving ability in DEVELOPMENT OF NEST BUILDING BY young male Village Weavers that had been THE MALE VILLAGE WEAVER completely deprived of normal nest material (Collias and Collias 1964, 1973) until almost one year of age. As yearlings, the Reports in the literature indicate that a bird controls not only tore more strips, they wove which was denied access to nest materials un- a significantly bigger percentage of their strips til it was an adult built a first nest that was (Collias and Collias 1973). However, both just like that of an experienced bird. This is groups wove by far the majority of strips on not true of the Village Weaverbird as we saw the wire of the cage-an easier place to weave in Africa. Males do not get adult plumage un- than on the twigs. In fact the deprived year- til their second year, and we saw colonies of lings didnt’ weave anything on the twigs. yearling males gathered in a tree practicing The next year, after considerable practice, building nests. The nest of a young weaver- the percentage of total strips woven by de- bird doesnt’ look much like the nest of the prived and nondeprived birds was not signif- Collias and CoZZiasl THE LIVING BIRD

FIG. 4. Typical sequence of movements by a male Village Weaver as he weaves a single strip of grass or palm leaf into his ring (Collias and Collias 1962). Drawn by Nicholas Collias from motion picture frames.

icantly different. However, the number of dominant bird has much more opportunity to strips woven on twigs was significantly dif- practice weaving. Since the young weavers ferent (Collias and Collias 1973). need practice in order to perfect the skills used When watching young Village Weavers in weaving the dominant birds actually per- learning to weave we have often seen a sub- fected their weaving skills and often went on ordinate tear a strip and immediately have it to build a nest at a much earlier age than did taken away from him by a more dominant the subordinate birds. bird. The dominant bird often then used this When matched with control birds that had strip to weave. Of course this means that the a similar dominance level, the deprived young 40 THE WILSON BULLETIN - Vol. 110, No. I, March 1998 wove a significantly smaller percentage of were built with any help or incentive from us their strips (Collias and Collias 1973). The de- so he had learned to build a very long en- prived birds in this case were only partially trance tube after he became an adult. deprived in that they had access to nest ma- In conclusion, our experiments on devel- terial until they were seven weeks old and opment of nest building by the Village Weaver then were not given any nest material until the showed: age of about one year when this test was done. A long-term example of the effect of lack (1) Self-reinforcement of inherited acts of practice on subsequent ability to build a with experience. nest was Male LL who was at the bottom of (2) Building a species-specific nest re- the peck order in his group which had been quires practice but not a tutor. completely deprived of nest materials after (3) A young bird has a long sensitive pe- seven weeks of age. He would tear a strip only riod (months) for nest building. to have it promptly taken away by one of his (4) Adults can learn new building habits. cage mates. As a result Male LL had almost INHERITANCE OF EGG-COLOR no chance to practice weaving, and never POLYMORPHISM IN THE learned to build a nest. He lived seven years, VILLAGE WEAVER and spent several breeding seasons in a large outdoor aviary with a number of the other Now I am going to shift from the building weavers. He changed to full breeding plumage of a nest to egg-color polymorphism in the each breeding season and held a territory, yet Village Weaver. It seems a bit far from be- in all that time he never managed to build a havior but as Ernst Mayr (1958) has pointed nest. He would tear a strip and taking it to a out, behavior often precedes related morpho- perch spend hours playing with it but he never logical evolution. wove one strip. Thus weavers must have suf- Most birds in North America lay only one ficient opportunity to weave when they are color of egg, but that is not true of the Village young or they never learn to weave. Weaver, the eggs of which vary widely in both Our colleague Cathy Jacobs who helped us color and spotting. The four background col- a great deal in our studies on weaverbirds ors found in the Village Weaverbird are white, hand-reared a male Village Weaver she called turquoise, emerald turquoise, and emerald. Phineas. Cathy kept Phineas in her office for Each female lays the same type of eggs over four years in a cage. Starting at about six her lifetime (E. Collias 1984). months she supplied Phineas with many long For fourteen years we did experiments that strips she tore from palm fronds, at least once required the female to make a choice between a week for a year and occasionally after that. the nests built by the males. To maximize the He often wove his strips on the wire cage and number of choices that females made we re- wove a complete ring his second year. At four moved the eggs of a clutch one or two days years he was put out in the large outdoor avi- after the last egg was laid. Each egg was iden- ary. This aviary was supplied with a fresh tified as to the female who laid it, the date palm frond daily for all the weavers. Phineas laid and the male to whom the female was was unable to tear a single strip by himself mated at that time. although he did weave a crude nest from strips By this method we accumulated well over he took from other weavers. This shows that a thousand eggs. Suddenly one day I realized not only rather complicated weaving requires that now I had an opportunity to explore the practice but also the more simple task of tear- genetics of egg color in a passerine bird (E. ing a strip. Collias 1993), something that had never been We induced an adult male weaver (RR) to done before, for in addition to having the build an abnormally long entrance tube on his eggs, we had been breeding these birds for nest by adding dangling strips with one end years and knew the parents and sibs of all our fastened to the entrance of his nest. Thereafter birds except, of course, our original flock. I although he usually built a normal length tube identified the color of each egg from the Vil- he sometimes built a long one several times lalobos Color Atlas which divides the spec- the normal length. None of these later nests trum into 33 hues and then subdivides and --- J --I-‘ -- - THE LIVING BIRD 41 grades them by chromaticity (the amount of Two Pairs of Allelesat Two Loci EeTt attenuation of the hue) and lightness (from Emeraid- black to white). For example, examination of variation in 59 eggs laid by female ABA over nine years showed that all her eggs were of turquoise hue, most were fairly light in color (Grade white Turquoise Emerald- 17), intermediate in chromaticity (Grade 6), ee9t-t ee,Tt turquoise and all were unspotted. Ee,Tt From 20 different crosses between 13 males FIG. 5. Example of matings by Village Weavers and 15 females which resulted in at least one and colors of eggs laid, consistent with hypothesis of daughter from whom we also obtained eggs, a pair of alleles at each of two autosomal loci, with I postulated five hypotheses as to the inheri- turquoise allele and emerald allele dominant over tance of egg color: two, three, or four alleles white allele but not over each other (emerald-turquoise at one locus, or two pairs of sex-linked alleles, egg; E. C. Collias 1993). or two pairs of autosomal alleles at two loci. On checking each hypothesis against the data quoise (ee, Tt) eggs, the other laid em- I ruled out the first four. erald turquoise eggs (Ee, Tt). Since space is limited, I will summarize the Therefore, these results are consistent with hypothesis that appears to explain the inheri- a hypothesis of two pairs of autosomal alleles tance of egg color and recommend that for at two loci for the inheritance of egg-color more details on the crosses, how I tested the polymorphism in the Village Weaver. hypotheses, and my reasoning with regard to Now why do Village Weavers have so acceptance or rejection, one can check my many different kinds of eggs? Our colleague, 1993 paper in The Auk. Janice McLean, answered that question. She The last hypothesis for the inheritance of put other weaverbird eggs into a nest already egg color is two pairs of autosomal alleles at containing eggs. Unless the added egg very two loci and postulates the following: closely resembled that of the host the strange Emerald-at least one dominant gene for eggs were immediately tossed out regardless emerald (E-), and only recessive genes for tur- of whether the added egg was the odd one in quoise (tt). the clutch or if the females’ own egg was the Turquoise-at least one dominant gene for odd one (Victoria 1972). turquoise (T-), and only recessive genes for This egg variability probably arose as a de- emerald (ee). fense against nest parasitism. Did this develop Emerald turquoise-at least one dominant as a defense against intraspecific or interspe- gene for both emerald and turquoise (E-T-). cific parasitism? I do not rule out either com- White-only recessive genes at both loci pletely. However, I do not think intraspecific (ee, tt). parasitism played a big part in the Village This hypothesis worked in all 20 crosses. Weaver. We never saw any evidence of this The other four hypotheses fail to explain the type of egg parasitism in three breeding sea- data. sons in Africa. However, it does occur. Janice, I shall give an example of how Hypothesis in four years of observation in our aviaries 5 worked-two pairs of autosomal alleles at saw two cases both under rather unusual cir- two loci (Figure 5): cumstances. In one case where the eggs dif- fered, the strange egg was ejected. In the other Male 1 (Ee, Tt)-mated with Female 1 who case in which both females had very similar laid emerald turquoise (Ee, Tt) eggs. eggs, the parasitic egg was accepted. They had a daughter who laid white (ee, I think interspecific parasitism probably tt) eggs. played an important role because of the work Male 1 (Ee, Tt)-also mated with Female 2 of Cruz and Wiley (1989) on the Village who laid white (ee, tt) eggs. They had Weavers which were introduced into Hispan- two daughters one of whom laid tur- iola by the early 18th century. These weavers 42 THE WILSON BULLETIN l Vol. 110, No. I, March 1998 were without brood parasites until the 1970s COLLIAS, E. C. 1984. Egg measurements and colora- when the Shiny Cowbird (Molothrus bonar- tion throughout life in the Village Weaverbird, Pbceus cucullatus. Pp. 461-475 in Proc. 5th Pan- iensis) arrived and laid in the weaver nests. Afr. Ornithol Congr. (J. A. Ledger, ed.). The weavers did not reject the cowbird eggs COLLIAS, E. C. 1993. Inheritance of egg-color poly- although these were quite different from the morphism in the Village Weaver (Ploceus cucul- weaver eggs. Evidently weavers had lost the lams). Auk 110:683-692. egg rejection behavior in the intervening 200 COLLIAS, E. C. AND N. E. COLLIAS. 1957. The response yrs, which they certainly would not have done of chicks of the Franklins’ Gull (Larus pipiwcan) to parental bill-color. Auk 74:371-375. if intraspecific nest parasitism was common. COLLIAS, E. C. AND N. E. COLLIAS. 1964. The devel- To summarize egg-color polymorphism in opment of nest-building behavior in a weaverbird. the Village Weaver: Auk 8 1:42-52. COLLIAS, E. C. AND N. E. COLLIAS. 1973. Further stud- (1) Each female weaver lays eggs with the ies on development of nest-building behavior in a same color characteristics all her life. weaverbird (Ploceus cucullatusj. Anim. Behav. (2) The inheritance of background color of 21:371-382. eggs is consistent with a hypothesis COLLIAS, E. C. AND N. E. COLLIAS. 1978. Nest build- of 2 autosomal alleles at 2 different ing and nesting behavior of the Social Weaver loci. Philetairus so&s. Ibis 120: 1-15. (3) A female will throw out any egg that COLLIAS, E. C., N. E. COLLIAS, C. H. JACOBS, E MCALARY, AND J. T. FUJIMOTO. 1979. Experimen- differs markedly from her own eggs, tal evidence for facilitation of pair formation by a protection from brood parasitism. bright color in weaverbirds. Condor 81:91-93. (4) This favors selection for uniformity of COLLIAS, N. E. 1943. Statistical analysis of factors eggs of the same female and vari- which make for success in initial encounters be- ability between females. tween hens. Am. Nat. 77:519-538. COLLIAS, N. E. 1950. Hormones and behavior with Our research on bird behavior has given us special reference to birds and the mechanisms of much enjoyment and intellectual satisfaction hormone action. Pp. 277-329 in Steroid hormones over the years, as has the consequent inter- (E. Gordon, Ed.). Univ. of Wisconsin Press, Mad- action with many friendly and helpful students ison. COLLIAS, N. E. 1952. The development of social be- of birds. Foremost among the latter has been havior in birds. Auk 69: 127-159. Margaret Morse Nice and the inspiration and COLLIAS, N. E. 1962. Social development in birds and guidance given by her research on the life of mammals. Pp. 264-273 in Roots of behavior (E. birds in nature. Bliss, Ed.). Paul B. Hoeber, New York. COLLIAS, N. E. 1963. A spectrographic analysis of the LITERATURE CITED vocal repertoire of the African Village Weaver-

ALLEE, W. C. AND N. E. COLLIAS. 1940. The influence bird. Condor 65:517-527. of estradiol on the social organization of flocks of COLLIAS, N. E. 1987. The vocal repertoire of the Red hens. Endocrinology 27:87-94. Junglefowl: a spectrographic classification and the ALLEE, W. C., N. E. COLLIAS, AND C. Z. LUTHERMAN. code of communication. Condor 89:5 10-524. 1939. Modification of the social order in flocks COLLIAS, N. E. 1991. The role of American zoologists of hens by the injection of testosterone propionate. and behavioral ecologists in the development of Physiol. Zool. 12:412-440. animal sociology, 1934-1964. Anim. Behav. 41: ANDERSSON, M. 1994. Sexual selection. Princeton 613-631. Univ. Press, Princeton, New Jersey. COLLIAS, N. E. 1997. On the origin and evolution of BARTHOLOMEW,G. A., E N. WHITE, AND T R. HOWELL. nest building by passerine birds (Passeriformes). 1976. The thermal significance of the nest of the Condor 99:253-270. Sociable Weaver Philetairus socius; summer ob- COLLIAS, N. E. AND E. C. COLLIAS. 1956. Some mech- servations. Ibis 118:402-410. anisms of family integration in ducks. Auk 73: BUNTIN, J. D. 1996. Neural and hormonal control of 378-400. parental behavior in birds. Advanc. Stud. Behav. COLLIAS, N. E. AND E. C. COLLIAS. 1959. Breeding 25:161-213. behavior of the Black-headed Weaverbird Textor BURGESS,T W. 1919. The Burgess bird book for chil- cucullatus graueri (Hartert) in the Belgian Congo. dren. Little, Brown and Company, Boston. Ostrich (suppl.). 3:233-241. CAREY, C. (ED.) 1996. Avian energetics and nutrition- COLLIAS, N. E. AND E. C. COLLIAS. 1962. An experi- al ecology. Chapman and Hall, New York. mental study of the mechanisms of nest building CHAPIN, J. I? 1954. The birds of the Belgian Congo. in a weaverbird. Auk 79:568-595. Part 4. Bull. Amer. Mus. Nat. Hist. 75B. COLLIAS, N. E. AND E. C. COLLIAS. 1963. Selective Collias and Collias l THE LIVING BIRD 43

feeding by wild ducklings of different species. CRAIG, A. J. E K. 1980. Behavior and evolution in Wilson Bull. 75:6-14. the genus Euplectes. J. Ornithol. 121:144-161. COLLIAS, N. E. AND E. C. COLLIAS. 1964. The evolu- CRAIG, W. 1911. Oviposition induced by the male in tion of nest-building in the weaverbirds (Plocei- pigeons. J. Morph. 22:299-305. dae). Univ. Calif. Publ. Zool. 73:1-162. CROOK, J. H. 1962. The adaptive significance of pair COLLIAS, N. E. AND E. C. COLLIAS. 1967a. A quanti- formation types in weaver birds. Symp. Zool. Sot. tative analysis of breeding behavior in the African Lond. 8:57-70. Village Weaverbird. Auk 84:396411. CRUZ, A. AND J. WILEY. 1989. The decline of an ad- COLLIAS, N. E. AND E. C. COLLIAS. 1967b. A field aptation in the absence of a presumed selection study of the Red Junglefowl in north-central India. pressure. Evolution 43:52-62. Condor 69:360-386. DARLING, E E 1938. Bird flocks and the breeding cy- COLLIAS, N. E. AND E. C. COLLIAS. 1968. Annas’ cle. Cambridge Univ. Press and MacMillan, Co., Hummingbirds trained to select different colors in New York. feeding. Condor 701273-274. DARWIN, C. 1871. The descent of man and selection COLLIAS, N. E. AND E. C. COLLIAS. 1969. Size of in relation to sex. Photoreproduction in 1981 by breeding colony related to attraction of mates in a Princeton Univ. Press, Princeton, New Jersey. DARWIN, C. 1872. The expression of the emotions in tropical passerine bird. Ecology 50:481-488. man and animals. Philosophical Library, New COLLIAS, N. E. AND E. C. COLLIAS. 1970. The behavior York (1955 reprinting). of the West African Village Weaverbird. Ibis 112: EMERSON, A. E. 1938. Termite nests-a study of the 457-480. phylogeny of behavior. Ecol. Monogr. 8:248-284. COLLIAS, N. E. AND E. C. COLLIAS. 1971. Ecology and FABRICIUS, E. 1951. Zur Ethologie junger Anatiden. behavior of the Spotted-backed Weaverbird in the Acta Zool. Fenn. 68: 1-178. Kruger National Park. Koedoe 14: l-27. FLINT, E. N. AND K. A. 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