ek. pare e PV etn Lie Pa Myce eS RL eu F $: wh ha. yt es aa t iy Ai Lh Dee ee a A AC LA hae The person charging this material is re- sponsible for its return to the library from which it was withdrawn on or before the Latest Date stamped below. Theft, mutilation, and underlining of books are reasons for disciplinary action and may result in dismissal from the University. UNIVERSITY OF ILLINOIS LIBRARY AT URBANA-CHAMPAIGN USE ONL v IQ7A wig & L161— O-1096 by = — 1G Digitized by the Internet Archive in 2011 with funding from University of Illinois Urbana-Champaign http://www.archive.org/details/parentalcareitse22kend \ in ef). Meg Hhinos Biological M onographs VOLUME XxII University of Illinois Press URBANA BOARD OF EDITORS Harley Jones Van Cleave H. Orin Halvorson William R. Horsfall Leland Shanor Aubrey B. Taylor CONTENTS Nos. 1-3 Parental Care and Its Evolution in Birds S. CHARLES KENDEIGH No. 4 The Leguminosae of Illinois WILLIAM G. 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[Continued inside back cover] | PARENTAL CARE AND Its EvoLuTIon IN Brirps ~ a iH e nee pa —- ae ery tg t em a x in F set . le ‘ ee , *¢ a ies e mA a roae 7 +e BO a ) - ¥ = Js ae = . eins g te : > : ' ao - ~ > : = es » } | on as iy * ry cng : 7 as ' ut Ay ue —_ a « @ . 7 h 7 - 7 y re , - - . 3 - - < a x : 7 © @ oF — ’ = TR : ~] = x ? “ a) 7 ‘ ' 2 - & Parental Care and Its Evolution in Birds S. CHARLES KENDEIGH ILLINOIS BIOLOGICAL MONOGRAPHS: Volume xxu, Nos. 1-3 THE UNIVERSITY OF ILLINOIS PRESS URBANA, 1952 Copyright 1952, UNIVERSITY. OF ILLINOIS. MANUFACTURED IN THE UNITED STATES OF AMERICA. Board of Editors: HARLEY JONES VAN CLEAVE, H. ORIN HALVORSON, WILLIAM R. HORSFALL, ROBERT E. JOHNSON, AND OSWALD TIPPO LIBRARY OF CONGRESS CATALOG CARD NUMBER 52-5887 Contents I, TENPTORMCTOLONCHIST CIN facies ap ca ee oes ar ee Se 1 SIMENTERHODSMORSSDUDY. © ine ie Gtk pee la oes a Boas PS y OL ise wtens 5 IMechamicaleNicthods'|s ei-t1.6s ecu ane feacd sie ae dae dae eee ae ced 2 Thermocouple and potentiometer................0..000005 5 > Perch contacts and..electromagnet.................0200+5-+> 6 2 RHGtOe ECUTICNCEIENs an sui. fdesiGhed-s os ea ng eo tee tee em eS 10 vO Observational Methods 44.5 6s (Gein ow cs te eae oe ee eee 10 ay Presentation and Evaluation of Data. ..........6. 268.05 s+00 12 II. ATTENTIVE BEHAVIOR OF THE HOUSE WREN..........-0++++00055 14 Territorial Activities of the Male at the Nest Site.............. 14 Nesta bullaine by the Female. cc... nace ois ie dee oe ce ee 18 Meme Tavine” (RETO. iu i0o< etaat OY Sea. eee os eS ea 19 4 MMe ACOMPeTIOW Ut Gite clita eels a6 «ve ee ae Sees gees bin wees 26 | Comparison of potentiometer and itograph records........... 26 @hances with progress of incubation.c5..6.00. 666 55s 0s een 27 Averages for individuals and the species.................... 40 Changes with age, mates, and season...............-000055 40 ‘ imbwence oF airs temperature: 2450. Ja .a5 ss wah eens che 8 Ae 40 \ Correlation with length of incubation; :...%.0..4.:% +666. .4.+ 43 My Influence of male on the female’s behavior................. 44 ~ Relation between number and length of periods............. 46 IBLOOGdING (Ene YOUNG. 12, os 440s. 0h on eeee be bas «ge hnse waive 49 RS HeCGING tHe PY OUNG he graces Cains ow wh hae s tw Hea aaa ea! ‘\ Ghanees wath: erowth: Of YOUNG an. weiss ee OA otis a ee 59 : Relation to number of young in nest... 02: 2+... ee ee eee de 61 Relation to length of nestling period.................+-000: 66 Relation to: OtherelactOrs. .. 4282 a5 7een eee tee sae oe neh ame 66 \ PA ECC TALLY CWO CTIOOS te Orrin a hc ay ding seas Ile ahead aidye ee sere 67 NV Daily- Rhythm im Attentive. Behavior. ....4.--...20. 6.06. -205- 69 oS Wile seomaver. (iseSter cigar a ce aie cea ttane et eae ere Barone meet eee 69 IN@sE -bumlding. by. feniale 2252. 7) 2. 2 bated Gace bow dnc a sudaw s a6 70 OOS yal Oe ante ca Wake, sie 5 Soin eee mos ab eres aes oucds ieee eats Beene e ate 70 i avehed ayn (oly eee aCe ea ane eee re Mo eae ge ed Ne aa ec ie Vi PARENTAL CARE AND ITS EVOLUTION IN BIRDS Influence of temperature. .i'..2...09is4..0 $0 0 eee Brooding <.5..9.5s 2 Gis wen are Melee ee re ee Feeding the: yourtg 3 te... «. 4nh eet ee eee 3 Time of Beginning and Ending the Day’s Activities............ Activity at Night”... ¢.2.-..0%5..4.4...0%. ated oso ue 2 Discussion ted s Qos aca ne oie occas Seta ns Stas soe eee SUIMMALY, heh ge soe iene ane bin wal Oy Siecle eed) aon IV. ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES........ Peers! Killdeer, Charadrius (Oxyechus) vociferus:.... ..2c fp Chimney Swift, Chaetura pelagica.. <. 205.0. 25... se Belted Kingfisher, Ceryle (Megaceryle) alcyon................ Flicker;: Colaptes auratus: 235 233.200. We. oe ee Crested Flycatcher; Myiarchus Crinitus. 0.022. 2 oe Phoebe; Sayornis. phoebe... cin. 22's 2<'ou Dates Gee Wood Pewee, Contopus (Myiochanes) virens.................4. Barn Swallow, Hirundo rustica (erythrogaster). ................ Purple ‘Martin; Progne*subis: os. hae se at Se ee Catbird; | Dumetella carolinensis... v2. :,0.:. «5 2 oe American Robin,. Turdus. migratorius ...03.... 0c \o02 . cutee Wood Thrush, Hylocichla musteling. . uci... hous ss is ee Hermit Thrush, Hylocichla: guttata.. 028s. 2. eee Bluebird,.:Sialia“stalis ns Sc hak ones ee Cedar Waxwing, Bombycilla cedrorum... >... 0'. oo shee — Yellow Warbler, Dendroica petechia (aestiva)...............%. Goldfinch; Spintis: tristisec..s ens 26 sctwtd os ea ee Chipping Sparrow, Spizella passerina.. 25 20s. eo ee ee Song Sparrow, Melospiza melodia. .....2' 7). saites os eee Singing: oF the male 25.065 %..0he acum gs ss 6 Sere eae ee Nest buildingof the female. 2... 0. 7.0. ohn see oe ee ESO laying my, a0h: Sete ested ac eitaaees anche hee oe ike Incubation:-.. te, Ache Gc nz Bios S53 e 0 A es ee eee Broogin’ “VOUNGE <. secs oie esata eas 2 Bee eee nd Oe ee Heeding young. ..2°ii eis ch pte bes cs Boe ek See Daily: rhythm. o0e «fone bea nen ee Oe ee Bee ee Beginning and ending of day’s activities: .°).s..0..... ose me Activity: at Micht 22 on3 ose See ans ee ae Discussion’ and Sumimaryso34 oases co Oe beac ee eae oe eee V. “EVOLUTION: OF PARENTAL GARE: 02... 2eno8's ced a ee ee Introduction: 420045. techs elie aes - eee oe nee ee Superorder: Palaeognathae; Order: Struthioniformes........... Family: Strathionidaé 2s #5 22 Sho. eee 39 101 102 109 137 140 175 175 CONTENTS vii Oren we mormress ke eicee ae 88 o hears ele abe wieaela Min aetae ee cae io FATT MMIR LC TOLAC WA cs oit-et clas oie not toad «ne, Coane Sat eee ae eee ieee 175 O@rcene@asuraiiformes fis... is Osa she bee eS cee 176 eMimill ee DTOMMCEH GAGs» iss.
Family: Fregatidae « .)+.. 0:22.02 ..%6:55 183
RODD CAWG CE Gly Meme oh ype ote One ne oR Poe eae 183
Order CicOnMEOUMeS. « 4 29a iene yaa ies oe gathows 6 eRe grees Ge RRS 183
Suborder» Ardeae; Family: Ardeidaé ..... .0.. 04.02 cece oes 183
Suborder: Ciconiae; Superfamily: Scopoidae; Family: Scopidae 184
Superfamily: Ciconioidea; Family: Ciconiidae.............. 184
Superfamily: Threskiornithoidea; Family: Threskiornithidae... 184
Suborder: Phoenicopteri; Family: Phoenicopteridae.......... 185
SIRI UI eee eh as, sence te earns Vania ea titge Gets cea reroute “cateer atie, ony > 185
Onder:e ANISCMIEOEMICS, shaun eaten Mic as ns tai sekoin eta ss ee ena oe ws 185
Suborder: Anhimae; Family: Anhimidae...............:.. 185
Suborder: Anseres; Family: Anatidae. ... 2: ....¢.65.0-.5555 186
SS UETAMIRU UG arrest ey ey Peed tea Crude Stee osc, fcr eo itr NERO eee ncaa met oe ack 188
Or er, Hal COMM OTINT CS ew cle ess ses ok lode esate: see dare hese liobare afaudasoary 189
Vill PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Suborder: Falcones; Superfamily: Falconoidea; Family: Accipi-
tri ae® aoa ie sa boc: & genial ahi Seen tins of easy sce aa a 189
Family: Falconidae 2.7) 3.9525. ars. Pes ee eee 192
Summimary =." esc Sek scans eee Spoon Roane One ERE eps REO 193
Order: Galliformes. .2s (20.225. 2 Ue Sn eee ee eee 193
Suborder: Galli; Superfamily: Cracoidea; Family: Megapodiidae 198
Family>-Cracidae.),..c. 0g. ci noe ti ak Seo a ee 194
Superfamily: Phasianoidea; Family: Tetraonidae........... 194
Family: Phasianidae ~ <5 22s.c0 0. tae oe: 0. eee 195
Family: “Meleagrididae’. .. 02.052..00. 025) =]: 2 eee 197
Suborder: Opisthocomi; Family: Opisthocomidae........... 197
Summary. +) Jes 2)iaeSdewstad Sco wie G cya Soe eee een 197
Order: (‘Gruiformes 4.) FP Ae oe Se ee 198
Suborder: Mesoenatides; Family: Mesoenatidae............ 198
Suborder: Turnices; Families: Turnicidae, Pedionomidae..... 198
Suborder: Grues; Superfamily: Gruoidea; Family: Gruidae.... 198
Superfamily: Ralloidea:’Family:: Rallidae 322.2 shee 198
Suborder: Rhynocheti; Family: Rhynochetidae............. 199
Suborder: Eurypygae; Family: Eurypygidae............... 199
Suborder: Otidés; ‘Family:Otidae 4, 7. 2.2% Scene eee 199
Summary fe .2ss ay dicen cet Se ele aioe ee sake, Sts eecab oes er ne ene ee 200
Order: Gharadriiformes 5.5) 2s see safe es ee 200
Suborder: Charadrii; Superfamily: Jacanoidea;. Family: Jacani-
(6 F - a e oer B A era eh Pe MOE Nats ER do So 6 c 200
_ Superfamily: Charadrioidea; Family: Rostratulidae......... 200
Family:. Haematopodidae®; 4.0 sas Yvan toda de kee 200
Family: ~Gharadnidae 2) oo oo os Se eee 201
Family; “Scolopacida@s: $..2 202% ...,. > ston os on oe eee
Family: Recurvirostidae.45 i.) 04.2 sae eee eee 203
Family:-Phalaropodidaés. 3 225-i4.-aee ooo ee eee 203
Superfamily: Burhinoidea; Family: Burhinidae .. .......... 203
Superfamily: Glareoloidea; Family: Glareolidae............ 208
Superfamily: Chionidoidea; Family: Chionididae........... 204
Suborder:Lari; Family: Stercorarlidacé: 22/44. .< 4.14745 eee 204
Family saridae tec. 9.2) ois Petes askcie as cdc ee 204
Family: Rymchopid dete «./dta Snaa hale ahtey oe oes ae ee eee 206
Suborder: Aleae; Family: Alcidde’.:. ...% 025 ts no eee 206
SUMMATY Ven = aelnwed oe ae Cok we OS eS nual s eee ee ee eee 206
Order: Columbiformes tess tc se. pterci oe ne ee ae ee 207
Suborder: Pterocletes; Family: Pteroclididae .. ...........4: 207
Suborder:- Columbae;. Family: Raphidae?.3.. 2.3.4 52 2 eee 207
Family: Columbidae:? 2.4 Vias 1a. acuee ei aren oe eee 208
SUMINIALY sv ug ee reeiie Mt Seda el Geet 4 ons ASE Petpet eee pe aise etree 209
CONTENTS ix
Org erm slitaCleOnMies, toes 8 See. fis a 2%. ¢ Goeus! Halarse a hepn Speed ings are 209
aM AMMSICACLO AGL. os fet hs fdas gat OR ea A ae oh ee 209
Orclernw CmcuWlOrmes os. fectls eo 6 55 4 dele es ps waste wee eee 210
Suborder: Cuculi: Family: Cuculidae ..2-.......2...5).5.- 210
SWUTCTOD AWAY 5. & 48 Pat SRR ern eh ert ra rl
(Omdiene | Siankeatio) nana, es sree ne 214
Blammily eum lytOrmC aes cee yaltiic ce owls Gib tie Salo ca Sl Ae ace ew Sal's 214
| Seammmuthys Saas EV ee Soci a oe ae 214
SUMMA ued gees oes se oe Ne Na ge yO Vor s.cee aio) BES Oe 216
Orderp CaprimuUlgitOrmes iess.5. 4 ec ara s ae cee eas as aw ne ee eos 216
erly Capri SAGAC wee ai winks ee 6 ae oS S ow a gle winks G 216
IS NULTOIDIVE TAY oc Ab SARS aan CP 217
Order vApOdiOrmes Shae. ies wd ee ce Fda bene eeews 217.
Suborder: Apodi; Family: Apodidae . Re Oe fort eee eal
Suborder: Trochili; Family: Treculidee. Bee ro a ee eee L
SUM UVP PW Mee Io ie a Owe we ae Seer Oe ae hs eaea ns oe
Order aro VOmirOrmes «i026. 54 68 eG ea pase en bd dawn ee ee 228
AT PAM ETOSOMIGAGy. A. 6 “ese eeclecie ds osu has ole wie ecueeie) LOO
Orde mOOraCiLONINesa-..c .o diaiee acs oe rode eNleeg wee Shoe to .8 2S
Suborder: Alcedines; Superfamily: Alcedinoidea; Family: Alce-
CHING AG Mripes Pl ee 50m 2s Gufs SM eae oO Seu it Mews ..eure eas DOO
Superfamily: Momotoidea; Family: Momotidae............ 224
Suborder: Meropes; Family: Meropidae.................. 224
Suborder: Coracit; Family: Coractidae..... ........0...+... 224
rary W ip UNDIGaC! Saupe ater ett aise ace wets wr a Wena s Amer OOS
Rammly® hocmiculidacan.-+.4m be4 eas eee «oe oka tbs. se eens, 220
Suborder: Bucerotes; Family: Bucerotidae................. 225
SS MMMM UI cess etre its CEN ee reneged tein cfd b's a 'iahthaw x ean DOO
Order puiCHOlnes 54. fie Mog ke hake esos ed bole ss orca ee 226
Suborder: Galbulae; Superfamily: Galbuloidea; Family: Gal-
| ciUULS LEYS as er ages aerera ana eae creas enc Utne ae eae eee: eS "4 5
Mamailyer BUCCOMIGaeGs .c.2, aes ada Gs 4p eats Sn sea Va hs oa 228
Superfamily: Capitonoidea; Family: Capitonidae.. ......... 226
aroily MndiCatonidaei. <4 22452 os sod emt nae cals ol aes ad satis 200
Superfamily: Ramphastoidea; Family: Ramphastidae........ Seva
Suborder: “Pict: Family: Picidaéx. . 4.022. 5) ....2.2.05<..3a0 227
OrderseLassevitOnmes! 5 1. tee sa cusses eye ast Ba ees os ote elo
Suborder: Tyranni; Superfamily: Furnarioidea; Family: Dendro-
COlADUC aC Ines eee. eine a a hse ee ones.) Panini en, OOO
analy: sMunnariidace.ci ) oO ee
VII. SPECIES INDEX
279
303
I. Introduction
The study of bird behavior is of intense interest to a great many people.
A few fortunate individuals are able to pursue this study vocationally,
but to most it can be no more than a hobby. Bird behavior is complex,
varied, and challenging at all seasons of the year. Each season induces
some different activity, such as migration, mating, nesting, molting, or
flocking. One must go into the out-of-doors to study these activities, but
he need not go farther than his backyard to find much of interest and
importance. Certain psychological analyses of how and why birds be-
have as they do and the testing of sense organs, reflexes, and conditioned
responses may be done in the laboratory, but it is necessary to study the
bird in the field under free, natural conditions to get normal behavior in
its full complexity and significance.
Early ornithological studies were concerned principally with making
collections of specimens, and with morphology, classification nomencla-
ture, distribution, and economic values. Buffon, of the eighteenth cen-
tury in Europe, and Audubon, of the early nineteenth century in North
America, were unique in opposing this emphasis and in compiling in-
formation on the life histories of birds and on natural history in general.
Toward the end of the nineteenth century and into the twentieth
century an increasing number of ornithologists gained prominence, in
part or in entirety, because of their attention to out-of-door studies of
bird behavior. In North America the following names come to mind:
William Brewster, Charles Bendire, Frank L. Burns, Frank M. Chapman,
Francis H. Herrick, Henry Mousley, Arthur C. Bent, Arthur A. Allen, to
mention a few. Bendire (1892) made an outstanding compilation in his
Life histories of North American Birds with special reference to their
breeding habits and eggs. This was the authoritative reference for a
long period. In 1919, an ambitious new series was begun under the
authorship of A. C. Bent which sought to include information on all
phases of the life histories of all species and subspecies of North American
birds. During the next thirty years, seventeen volumes appeared and the
series is not yet complete. Needless to say, Bent’s Life Histories have ex-
erted a tremendous influence and stimulus in ornithology.
Jourdain (1930) has traced the early development of interest in atten-
tive behavior in England and Europe. Three outstanding recent com-
pilations of life history information have been Die Végel Mitteleuropas,
prepared by Oskar and Magdalena Heinroth between 1924 and 1933;
Niethammer’s Handbuch der deutschen Vogelkunde 1937-38; and The
i
2 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Handbook of British Birds by H. F. Witherby, F. C. R. Jourdain, Nor-
man F. Ticehurst, and Bernard W. Tucker. The five volumes of this
last work were issued between 1938 and 1941.
These lengthy compilations are extremely useful in bringing together
in one place a vast amount of information on the life histories of every
species, in exposing the great vacancies in our knowledge of even the
most common species, and serving as a point of departure for the more
detailed, specialized approach of modern research.
The modern period of life history studies began about 1920 and is
characterized by the emphasis placed on such special concepts as
“territory” (H. E. Howard 1920, Nice 1941), “despotism” (Schjelderup-
Ebbe 1922), and “releasers” (K. Lorenz 1935, N. Tinbergen 1948); and
on the use of such techniques as bird-banding (Baldwin 1919, 1921)
and nest activity recording-mechanisms (Bussman 1924, Baldwin and
Kendeigh 1927, Kendeigh and Baldwin 1930, Kluijver 1933). In ad-
dition, there is an increasing effort being made to uncover the physio-
logical basis or conditioning influence on behavior (Rowan 1931, Ken-
deigh 1934).
Before the modern period, bird observers had frequently noticed how
incubating birds left the nest to get food for themselves and the fre-
quency with which they fed the young in the nest. It required me-
chanical recording, however, to demonstrate the regularity and length
of the periods on and off the nest during the incubation period and to
give emphasis to this phase of nesting behavior. Baldwin and Kendeigh
(1927) called these intervals spent on and off the nest, periods of at-
tentiveness and inattentiveness respectively, and emphasized the impor-
tance of this underlying rhythm throughout the reproductive period.
The periods of attentiveness are defined as those intervals of time when
a bird of either sex is actually engaged in nesting activities, whether
these activities be singing, nest building, incubating, brooding, feeding
the young, or scolding at enemies. Periods of inattentiveness alternate
with periods of attentiveness and are the time intervals devoted to feed-
ing, bathing, preening, or resting.
Essentially there are two basic drives involved, that of self-mainte-
nance or existence and that of reproduction. Attentive behavior is that
phase of life history wherein the interplay between these two drives
becomes expressed. Attentive behavior is nearly synonymous with par-
ental care except that it is concerned more with the time relations of
nesting activities, while parental care also includes other behavior mech-
anisms and relationships between adults and young. It is primarily with
the timing aspect of parental care that this discussion is concerned.
The house wren, Troglodytes aedon, is the species that will receive the
most detailed treatment in this study. The field data were collected
INTRODUCTION 3
primarily at the Baldwin Bird Research Laboratory, formerly located
at Gates Mills, near Cleveland, Ohio, during the years 1925 to 1939
inclusive. This species had long been the object of concentrated atten-
tion at this laboratory; it was numerous, its nests placed in boxes were
easily accessible, and considerable information of other kinds had been
worked out about it. The study of attentive behavior was part of the
program that involved a detailed comprehensive study of the life history
of the species.
Many other species were also available on the fifteen acres surround-
ing the laboratory, so as time was available for observations and as instru-
ments were free for registering nesting activities, attention was paid to
the attentive behavior of seventeen other species. Two additional species
were studied at the Edmund Niles Huyck Preserve near Rensselaerville,
New York.
Altogether, some 127 separate automatic recordings were made of
nesting activities of the house wren and some 39 recordings made of
other species. Usable data were obtained from some 1,075 daily 24-hour
records of the house wren and some 428 daily records of other species.
Probably the usable daily records constituted between one-half and
two-thirds of all those actually obtained, several of which were im-
perfect in one way or another.
The analysis of this large amount of data was no small task. The first
thing necessary was to convert the graphical record made by the auto-
matic recorders into time intervals that could be compiled, classified
in various ways, and from which averages could be made. The writer
had the help of several assistants over the years for the handling of the
records. Miss Mae McNab was especially helpful in devoting much
time to inscribing the hourly intervals on the original records. Student
assistants employed under the National Youth Administration during the
1930’s were largely responsible for converting the graphical record into
numerical tables and computing averages. Most of the computations were
made on an automatic calculating instrument and rechecked at least
once. The supervision of this statistical work and the final interpreta-
tion of the data were, of course, the author’s responsibility.
The review of literature bearing on this subject, especially in the sum-
mary of attentive behavior in the various families of the birds of the
world, was begun shortly after the study was initiated and kept more or
less up to date as new publications appeared. Several hundred reference
cards accumulated, and all of these references had to be consulted and
pertinent data compiled. Student research assistants were helpful in this
connection, although when the time came to the actual writing of the
summaries, the original literature often had to be consulted a second
time. The review of literature was essentially completed by January,
4 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
1950, and it.is believed that all important publications bearing on atten-
tive behavior up to that date have been consulted and listed in the last
section of this paper.
Finally, I wish to acknowledge the indispensable role of Dr. S. Prentiss
Baldwin in this study. Without him the study would probably never
have been undertaken. Dr. Baldwin organized and financed the Baldwin
Bird Research Laboratory, where I was employed as a research associate
for the summer periods of fifteen years. He had an unusually open mind
for new techniques and ideas in ornithological research, and, what is just
as important, was willing to devote time and money for developing them.
He had many stimulating new ideas of his own, and his constant day-
by-day contact with all phases of the work going on in his laboratory
was a continuous source of inspiration and encouragement. Dr. Baldwin
died on December 31, 1938. Had he lived, he would certainly have been
a joint author of this paper. As it is, this book is contribution No. 44 from
his laboratory, the Baldwin Bird Research Laboratory, Gates Mills, Ohio.
I wish also to express my indebtedness to Mrs. Margaret M. Nice, who
read the entire manuscript and offered many valuable suggestions and
criticisms. Chapter V was read by David Lack, of England, R. E. Moreau,
formerly of Tanganyika, South Africa, Alexander F. Skutch, of Central
America, and L. E. Richdale, of New Zealand. Each of these men is an
authority on the birds in his area and the world-wide coverage attempted
in the review of the literature on parental care has benefited from their
suggestions, from their citations to literature which I had overlooked, and
from unpublished data that they gave me. I hereby acknowledge my
obligation to them.
Department of Zoology S. CHARLES KENDEIGH
University of Illinois
I. Methods of Study
The extensive development of this study of attentive behavior was
made possible by the invention and adaptation of automatic instru-
ments to record all the visits of the parent birds to the nest. These
instruments permitted 24-hour daily registration of all trips and the
amount of time spent at and away from the nest. Observation alone could
not have amassed such a voluminous record without a prodigious ex-
penditure of time and expense.
MECHANICAL METHODS
The automatic recording of animal activity, including that of birds,
over long continuous periods has been practiced in the laboratory (Szy-
manski. 1914). Devising equipment for use out-of-doors presents special
difficulties, as it is highly desirable that the bird or animal be inter-
fered with as little as possible and that it lead an entirely normal and
natural existence. However, a number of methods have now been
devised or adapted for the automatic recording of trips made by birds
to and from their nests. These may be conveniently classified under three
different main types of equipment. The thermocouple and potentiometer,
and the itograph constituted the equipment used in the accumulation
of the original data of this report.
Thermocouple and potentiometer. Baldwin and Kendeigh described
in 1927 the adaptation of the thermocouple and recording potentiometer
to registering nesting activities. Details need not be repeated except
briefly to explain that the thermocouple is an electric circuit made of two
different metals, in this case copper and constantan, with a recording
potentiometer included in the circuit. The apparatus records temperature.
When heat is applied to one junction of the thermocouple and the other
junction is held constant, there is a difference in electrical potential
established with the resulting flow of a minute amount of electric cur-
rent. The potentiometer contains a sensitive galvanometer, a slide wire,
and a system of levers, cams, writing device, etc., to measure the flow of
electric current and record automatically in degrees of temperature the
amount of heat applied at the warm junction. The apparatus used was
purchased from The Leeds and Northrup Company, Philadelphia, Penn-
sylvania.
The warm junction of the circuit may be carried as far as 200 feet
from the potentiometer and placed so as to record the nest temperature.
The end of the warm junction is made in the form of a thin, flexible
5
6 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
wire which is threaded through the nest from one side to the other in
such a way that the junction itself lies just above or onthe eggs. The
visits of the adult are recorded when the incubating bird settles on the
eggs and applies heat to them. The departure is instantaneously recorded
by a drop in temperature.
The thermocouple will register a visit only when the bird applies heat
to the eggs. It will not record a visit to the rim of the nest only, nor the
time spent at the nest when not actually incubating. Obviously this
method is useful only during the incubation and brooding periods. The
thermocouple can be placed in almost any kind of a nest with little diffi-
culty. Recording potentiometers require electric current, however, and
this is a limiting factor. Indicator potentiometers, operated manually,
are available that do not require electric current, but there is little ad-
vantage in their use over observation.
Perch contacts and electromagnet. The itograph was first described
in 1930 (Kendeigh and Baldwin). It is based on quite a different prin-
ciple from the thermocouple and does not register temperature (Fig. 1).
The necessary parts are a double set of perch contacts at the entrance
of the nest, a set of dry-cell batteries, an electromagnet with a pen at-
tachment, and some means of unwinding a roll of paper at a uniform
rate. Two types of itographs were used in this study: a multiple type,
which had seven electromagnets and pens recording simultaneously on
a wide strip of paper that was unrolled by an electric motor in the
laboratory; and a portable type, which had a single electromagnet that
registered on a narrow strip of paper, unwound by a 48-hour clock, and
did not require connection to an electric current. It is possible to make
an efficient portable itograph using a doorbell for the electromagnet and
an alarm clock to unwind the paper (Hann 1937). The portable ito-
graph is light in weight and may be used almost anywhere in the field.
The itograph records all trips to the nest; it will therefore record nest
building and feeding the young as well as incubation. The total time at
the nest is registered, not just the time on the eggs.
The portion of the setup requiring special ingenuity in adapting to
the nest location is the double-perch arrangement. Two perches instead
of one are used so that the record will show whether the bird is enter-
ing or leaving the nest. The two perches are balanced on a central pivot
with springs so that the electric circuit to the electromagnet is closed
only when the perch is pressed down. On entering the nest, the bird will
press the outer perch down first, then the inner perch. This will swing
the pen attached to the electromagnet first to the right, then to the left.
On leaving the nest, the perches are pressed down in the reverse order,
and the pen will swing first to the left and then to the right.
Three sets of perches have so far been devised, as shown in figure 1.
METHODS OF STUDY
Front view Side view
Perch contacts jer boxes
MY
PURULENT
Recorder with
electromagnet Ferch contacts for Fivch contiers for
ground nests open nests
Itograph
Dry cell batteries
Recorder 7; lectromagnet
Terra graph
Fic. 1. Apparatus for the automatic recording of trips made by adult birds to
their nest. Both the itograph and terragraph use an electromagnet with a pen
attachment which writes on paper moved at a constant rate by a clock. The
itograph uses a double-perch arrangement that may be adapted to different
nest sites and which distinguishes between the arrival and departure of the
bird at the nest by the direction in which the pen is moved on the paper. The
terragraph uses only a single contact at the nest.
8 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
For such birds as house wrens that nest in boxes, the adaptation is fairly
simple with one perch just outside and the other just inside the small
hole through which the birds must enter and leave the nesting cavity.
With open nests, it is necessary to enclose all approaches to the nest
except one, and then build a short tunnel on that one side in which to
place the double perch. The enclosure is made of wire-mesh hardware
cloth. The perches may be varied in size to fit the bird. The third type
of perch has each of the two sections separately hinged in the middle
and is made low and flat so that it can be partly buried in the bottom
of a kingfisher’s nesting tunnel. For a comparison of data obtained dur-
ing the incubation period from the itograph and the temperature-
recorder, see pp. 26-27.
The terragraph is also an electromagnetic instrument and was in-
vented by a German, Count von Hegendorf, for studying the habits of
foxes and badgers. It was first applied to bird activities by Bussman
(1924, 1933).
The apparatus consists of a clock with a horizontal disk attachment 19 cm.
in diameter which makes one revolution with the clock in each twenty-four
hours. On this disk is placed a paper dial-plate marked with hours and half-
hours with a carbon paper on top, both being held in place by a tin disk
15 cm. in diameter, which is tightened by means of a central nut.
A telegraph magnet with a pencil attachment is stationed near the disk.
When the circuit is made, the pencil presses on the carbon paper, making a
short line 4 mm. in length on the paper disk beneath.
The contact at the nest consists of two small pieces of wood fastened together
at-one end by a flat steel spring (Fig. 1). This contact is placed in circuit
by means of insulated copper wire with two pocket batteries and the telegraph
magnet, so that when a bird alights on the contact the magnet records on the
paper disk.
This instrument is adapted primarily for recording the rate of feed-
ing the young in the nest, and several sets of data for different species
are given. A single mark is made in the record for each feeding trip as
the bird stands on the perch during the feeding process. The instrument
is less useful for recording attentive behavior during incubation, as there
is no distinction made in the marks to indicate whether the bird is coming
to or leaving the nest or whether the bird alights on the perch and then
immediately leaves. The most important difference between the itograph
and the terragraph is that the itograph does record the direction of
movement with its two marks.
Kluijver (1933) used a mechanical recording apparatus which he
called the aphisigraph, in his intensive study of the starling and later
of the great tit (1950). The perch contact appears very similar to that
used with Bussman’s terragraph. It was placed directly beneath the en-
trance to the nest cavity and recorded only the entrance of the bird to its
METHODS OF STUDY 9
nest. There was a second hole on the side of the box through which the
bird left. Trap arrangements prevented the bird’s going in or out in
the wrong direction. Ruiter (1941) also used an aphisigraph for measur-
ing the rate of feeding of young European redstarts.
Schantz (1939) used an electrical apparatus to announce or record
the arrival of robins at their nest. He does not describe the details of his
setup but states that it was impossible for the adults to come to the nest
without ringing an electric bell or making a recording on paper tape.
The mechanical registration of visits by the willow warbler to its
nest made by Kuusisto (1941) utilized an electromagnet and a pen writ-
ing on paper unrolled at a uniform rate by a clock and a system of
weights. He had two types of contacts at the nest. A thermo-contact was
a glass tube containing mercury with one end expanded like a thermom-
eter. Two platinum points were inserted in the tube so that, when the
bird applied heat on the nest, the expansion of mercury closed the
circuit. This contact was usable only when the bird was incubating or
brooding. It had certain disadvantages in that an egg would occasionally
get against the contact and insulate it against the heat of the incubating
parent, and in that one minute was required to warm the mercury suffi-
ciently to close the circuit. Kuusisto’s pressure contact was in the form
of a cradle or seesaw that closed a circuit momentarily when the
bird settled in the nest and again on leaving but did not distinguish
between entrance and exit. Koskimies (1950) used a modification of this
apparatus in his study of the swift, Apus (Micropus) apus.
Marples and Gurr (1943) also used a mercury contact at the perch,
but the closure of the circuit did not depend on a change in temperature.
The perch was similar to that used by Bussman, but the contact on the
lower half of the perch was a small cup of mercury into which a small
wire projecting from the upper half would dip when the perch was
pressed down by the weight of the bird. The two halves of the perch
were hinged at one end, and the upper half was supported on the lower
half at the other end by a spring adapted to the weight of the bird.
The recording mechanism differed in the use of a sharp-pointed lever
which was activated by an electromagnet to scratch a mark on the
smoked drum of a kymograph.
Nohring (1943) does not describe the self-recording device that he
used at one nest of the pied flycatcher, but apparently it included a
nest box constructed with a double floor, the upper one supported by
a spring which carried the weight of the nest and made a contact when
the bird entered.
Pullen (1946) installed an electric recorder at the nest box of a blue
tit which was operated by a very sensitive switch fitted in the entrance,
so arranged that passage of a bird, either in or out, was recorded as a
10 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
spot on a moving strip of paper. Gibb (1950) used a trigger at the
entrance to a nest of the great tit and an automatic counter of some
sort which is not described.
Photoelectric cell. An entirely different principle was used by Yates
(1942) in his recording of the visits of a house wren to its nest. “...a
photoelectric cell with a suitable six-volt lamp was installed and con-
cealed in such a manner that the wren had to cut the beam on each trip
she made for food. This interruption operated a relay connected with an
electrically-actuated counter.” This equipment would seem to have great
possibilities, especially if it were connected with a recorder rather than
a counter, but it has not been used extensively.
OBSERVATIONAL METHODS
Although there are many advantages in using mechanical recording
of nesting activities, direct observations should never be dispensed with.
Much can be learned through observations that cannot be recorded auto-
matically. The part played by each sex must be determined by obser-
vation, and also the number of young fed per visit to the nest. Other
behaviorisms associated with attentiveness need description, such as the
ceremony of nest relief, turning of eggs, sanitation, kind and amount
of food brought to young on each visit, feeding of incubating bird by
its mate, associated songs and call-notes, and similar items. Furthermore, |
direct observations should always be made to check the accuracy of
automatically recording devices. Instrumental technique requires con-
stant attention, adjustment, and checking; and the more the results
obtained from it can be verified by observation, the more reliable and
satisfactory they become. Birds often make unexpected movements or
have exceptional activities and, unless these can be checked through
observation, the interpretation of the record obtained from the apparatus
will be faulty.
Instrumental techniques have not yet been designed which are suit-
able for all species of birds, although the fabrication of such equipment
is a challenge to research workers interested in the quantitative side of
ornithology. This means that observational methods must be used en-
tirely if information on some species is to be secured. Further, it is not
always convenient or practicable to take apparatus into distant or less
accessible locations.
Blinds are often useful to enable the observer to be closer to the nest
and observe activities in greater detail. Herrick (1901) long ago de-
scribed the use of blinds, and various types of blinds have been em-
ployed since, both for close observations of nest life and for photography.
Very often, however, one does not need to use blinds but may obtain all
METHODS OF STUDY ll
the information he requires by sitting quietly at a distance and taking
his observations through a high-powered field glass.
All-day observations are very desirable, even if they can be carried out
only at intervals. As will be repeatedly shown later (Figs. 9-14), the rate
of activities at the nest varies greatly from hour to hour during the day.
Comparison of rates of attentiveness at different nests or by different ob-
servations on different species is not trustworthy if the information is
obtained at different times of day. All-day observations take in all these
hourly variations, give a more complete record of the species’ behavior,
and make comparisons more reliable. Usually, all-day observations require
the cooperation of two or more observers relieving each other at intervals.
R. E. Moreau was able to employ natives in Tanganyika, Africa, to ob-
tain observations over long continuous periods of time. The long hours
of observation by Otto Steinfatt at the nests of many species are also
noteworthy. In selecting the particular days for making all-day observa-
tions, one should keep in mind that the rate of nest building activity may
decline greatly after the first day; that the amount of attentiveness usually
increases day by day during the egg-laying period; that the rate of atten-
tiveness is fairly constant throughout the incubation period except for the
first and last days and as modified by pronounced changes in temperature;
that the amount of brooding after the young hatch progressively declines
after the first two or three days; and that the rate of feeding increases
as the young birds get older.
Often, it is not possible or convenient to take all-day observations.
Perhaps only a few hours are available. In choosing the time of day for
taking these observations, the usual daily rhythm of bird activities should
be kept in mind. Often the activity of the bird is unusually great or un-
usually low or modified in some way during the first hour or two in early
morning. It is well to avoid these hours if more nearly average rates are
desired. Normally, however, maximum activity occurs at some early
hour and then declines steadily to late morning or midday. During the
afternoon, activity is usually minimum but rises again in late afternoon
or evening. Probably the best time for observations of a few hours only
and for getting nearly average rates is between 0600 and 1200 hours.
The midday recession in the rate of the bird’s activity is less pronounced
or may actually be eliminated on cool days, so that similar data may
be obtained at almost any hour. On the other hand, activity may be-
come reduced on hot days. All of these variables need to be considered
in evaluating data and making comparisons. The description of the con-
ditions and circumstances under which the observations are made should
be as complete as possible in the presentation of the data.
12. PARENTAL CARE AND ITS EVOLUTION IN BIRDS
PRESENTATION AND EVALUATION OF DATA
Pitelka (1941) and Moreau and Pitelka (1943) have discussed the
proper presentation of attentive data. One important point emphasized
is that the data should be presented in table form. Details and important
information are often lost or obscure if given in the text of a publica-
tion. Graphs may supplement the tables but should never replace them,
as it is very difficult for the reader to compile statistics from a graph.
Furthermore, a certain amount of condensing and averaging of the data
by the author is desirable. The reader quickly becomes confused and
discouraged when he is required to work through the raw data as it
comes from the record or directly from observations.
Desirable information that should be presented includes the stage of
the nesting cycle, number and age of young, which sex of adult is active
or whether both are, length of record, time of day, and weather (es-
pecially temperature ). Data should be given for each sex on the average
length of the attentive and inattentive periods. It is not sufficient merely
to state the percentage of time the adult birds are attentive, as the length
of the attentive and inattentive periods cannot be computed from this
information. However, if the length of the attentive and inattentive
periods are known, the percentage of time that the bird is attentive can
be easily calculated, as can also the number of periods per hour. When
both sexes incubate, the attentive and inattentive periods are often of
equal length as one bird is on while the other is off. When neither sex
is on the eggs between exchanges, these average intervals should be
added to the inattentive period. If there is a ceremony at nest relief,
this should be described; also call-notes or other behaviorisms associated
with attentive behavior.
In respect to feeding the young, it is always desirable to know the
average number of trips to the nest by each sex per hour. It is not suffi-
cient to know only the average interval between visits. One cannot com-
pute the number of visits per hour from the average interval unless he
also knows the average duration of the visits. This knowledge is de-
sirable, but very often it is not given in the published reports of ob-
servers. Sometimes the feeding rate is stated on the basis of an entire
day, especially when comparative data are available for the whole
growth period. In these cases, the number of hours of feeding per day
should also be given so that the hourly rate can be calculated. The
assumption is usually made that young are fed on every visit, but this
is not always the case. It is desirable to know the average number of
young fed on each visit, and this may vary with the age of the young.
Additional points worth recording are amount of food given per feeding,
amount of brooding, and nest sanitation.
Periods of attentiveness and inattentiveness can be determined as long
METHODS OF STUDY 13
as the young are regularly brooded. However, with feeding only, they
are usually difficult to distinguish, especially if the feeding rate is fast,
although close study indicates that they still exist. Probably the analysis
of these periods should be based principally on the incubation period.
Attentive behavior is usually quite variable. It is worth while to have
some idea of the extent of this variability. This would be best shown
by the standard deviation and coefficient of variation, but these calcu-
lations are long and tedious and may not always be practicable. They
will not be employed in this study. As an alternative a statement of
extreme values has some usefulness.
Any reliable information, however scant, on the attentive behavior
of rare species is worth while. On common species a study of attentive
behavior should be based on more extensive data. Moreau and Pitelka
(1943) seem to agree that, with exceptions, the minimum period of con-
tinuous observation within any one day should be five hours. Actually
no such general statement is justifiable. In many orders below the
Passeriformes, a single attentive period during incubation or a single
inattentive period between consecutive feedings of the young may be
much longer than this. With such species, one needs to keep continuous
records at nests, either by observation or mechanical instruments, for
days at a time. But with species that have a fast attentive rhythm, even
two or three hours of observations are of value. Such observations should
be repeated, however, at the same time of day throughout the nesting
cycle to show changes with the stage of incubation or growth of young,
and should be repeated at various times on certain days to show changes
in the daily rhythm.
The daily rhythm in attentive behavior is conveniently shown during
the incubation period by the number of minutes each hour spent at
the nest, or it may be shown by the percentage of time spent in atten-
tiveness. During the feeding of the young, the number of trips to the
nest per hour is the most obvious method of presentation. We prefer to
consider the hour as extending from one-half hour mark to the next
rather than from the beginning of the hour to its end. This permits tabu-
lating and graphing the data on the even hour rather than on the half-
hour.
An important aspect of attentive behavior is the activity of the birds
at night, especially in regard to which sex incubates or broods, how soon
the adult starts spending the night on the eggs as they are being laid,
how late during the growth of the young she continues to brood, and
whether or not the adult leaves the nest at night or shows other restless-
ness. In this connection it is desirable to know for each sex the exact
time in relation to sunset and sunrise that the night period begins and
ends.
III. Attentive Behavior of the House Wren
Since more information is available on the attentive behavior of the
house wren, Troglodytes aedon, than on any other species, the concept
will be treated extensively in this species before comparisons are made
with other forms.
TERRITORIAL ACTIVITIES OF THE MALE AT THE NEST SITE
Since wrens nest in natural cavities or prefer boxes when they are
available, recording of their activities at the nest site is obtainable with
the itograph. A part of the procedure in establishing territories, along
with singing and fighting, is the finding and holding of anywhere be-
tween one and seven nest sites. The location of these nest sites helps to
outline the territory, and their possession is indicated by the insertion
of sticks, spider nests, and other materials that make up the nest founda-
tion. The male may visit all of his boxes each day. Neglecting to do so
permits the intrusion of other males and the loss of this portion of his
territory. The intruder may be challenged, but sometimes he is not.
Usually, the male is more active at some one preferred box than at others,
but the female, when she comes, may choose some other box for her
nesting than the one preferred by the male.
The need for regular attendance at all boxes in a male’s territory is
shown in the accounts of territories 153 and 154. The complete history
of these territories, as well as others listed by number in this paper, may
be found in Kendeigh (1941c). Male, L24956 was forced to care for the
young alone when the female deserted on June 15. This he did success-
fully, and the young left on June 25 and wandered outside the terri-
torial boundaries with the male attending them. This exposed his
territory to invasion by male 34-86085 from the adjacent territory. The
itograph shows that a bird, probably this invading male, made 49 visits
to the box on June 26. On June 27, the owner returned and attempted to
defend his possessions, but he was distracted by the need to feed his
young, and he lost in the competition. Altogether, 238 trips to the box
were made on this day by the two males. There was no disturbance of
the nest structure nor were there additions made to it; the males simply
went in and out at frequent intervals.
In repossessing a nest box that has already been used, the male re-
moves the nest lining that the previous female inserted and completely
cleans out the nest cavity. Then, when he obtains a new mate or the
14
ATTENTIVE BEHAVIOR OF THE HOUSE WREN 15
same mate a second time, she inserts fresh nest lining. The male ordi-
narily tears out the old nest lining with considerable energy and gusto,
singing vigorously. Usually two days are used for this task, but it may
extend over four days. The average of eight records on different males
gives an average of 113 trips to the nest each day.
Ordinary activity at a box to insure its continued possession is not in-
TaBLE IA. Activity of male house wrens alone at the nest box.
Ordinary activity
New (N) Number Average
Band or Year Terri- Box First of number of Extremes
number’ return (R) tory date days trips
record per day
A38398 R 1930 98 51 = June 23 t 22 4-67
A38398 R 1930 98 51 = July 12 6 25 12-42
A94242 N 1927 63 6 oe ae nee we
A94249 R 1928 75 11 = Junel 6 42 9-87
B97018 N 1929 90 9 June 16 13 24 3-45
B97018 N 1929 90 9 July 7 6 5 3-138
B97018 N 1929 90 49 July 2 17 12 2-35
C68252 R 1931 111 74, July 11 i 52 1-148
C68252 R 1932 122 53s July 12 3 19 6-26
Unknown N 1932-128 10 ~July8 6 59 14-133
C68800 N 1930 99 10 = June 22 8 50 31-127
C68800 N 1930 99 10. July 11 4 10 6-138
Unknown N 1930 103 68 June 22 6 43 19-70
C68801 R 1931 106 10 June 12 11 64 5-178
C68801 R 1931 106 30 )=6s June 19 5 Dia 12-154
C68801 R 1931 106 25 June 25 Us 34 4-184
C68910 R 1931 105 8A July 11 6 44 3-81
C68910 R 1931 105 10 = July 25 2 € 1-138
C68910 R 1933 = 129 49 June 28 aul 29 0-218
C68911 N 1930 96 25 July 20 6 2 1-9
F 45763 N 1932 =: 121 49 June 30 3 30 23-36
F45946 N 1932 «117 10. =June 18 3 36 6-91
F45946 N 1932 117 25 July 10 4 8 5-15
H18580 N 1933 126 10 July 2 8 28 9-76
H18582 N 1933 128 25 June 24 8 22 3-98
H18600 R 1934 141 25 July 12 18 12 1-25
L24956 N 1934 139 10 =June9 5 30 12-63
L24993 N 1934 140 10 June 17 4 60 33-106
35-13634 N 1936 164 53. June 6 8 14 0-77
35-13634 N 1936 §=164 538s July 3 14 10 0-39
35-13634 N 1936 = 164 49 July 4 13 8 0-22
16 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
TABLE 1B. Activity of male house wrens alone at the nest box.
Removing nest lining
2 i ae
Ee 9 Se tae : . me EE
S 3 iS) DQ. o SEO > Sr
= 3 ge bo 2 5 63,9 52 Ew
z = Bn aa Ea Boe HS) aS)
S Z se bee 5 Ses) oe
a cS PR eee cS a 8.2 >) cer ees
A38398 July 9 1 167 43 5.4 6.5
A94242 June 19 1 86 oe:
A94249 May 30 2 112 95-129 10 9.0 10.6
B97018 July 13 4 75 36-107 23 9.0 14.6
C68252 July 14 1 65 ae 18 3a 43.8
F45763 June 28 2 81 79-83 33 4.8 14.7
H18580 June 30 2 196 146-245
H18582 June 30 2 121 75-167 21 4.8 34.3
tense. An average of 30 records on 18 different males gives 29 visits per
day (Table 1), but the number is variable. This average may be some-
what high, as itograph connections were not often made to a box where
there was evidently little or no activity. When the male is busy carrying
in sticks or is excited by competition and singing, the number of trips
to the box may exceed 100. At other times, days may be skipped with
no-visits or only a very few. Sticks may or may not be taken to the nests
on these infrequent visits, and it is not practicable to divide the activity
of the male during this period on the basis of whether or not additions
of nest material are made.
There is a tendency for return males that nested the preceding year
to be more active than new birds nesting for the first time. The number
of trips to the box per day, however, is only 34 and 25, respectively, and,
with the variability noticeable, this difference is probably not very sig-
nificant.
Itograph records were simultaneously obtained in three instances at
two boxes in the territory of a single male. With B97018 in territory
90, the male averaged 5 visits per day at one box and 12 at another.
Male C68801, in territory 106, averaged 64 visits at one box and nearly
the same, 57, at another. Likewise, with 35-13634 in territory 164, the
average numbers of trips to each of two boxes were 10 and 8. In terri-
tory 117, male F45946, had a female with a nest in box 26 and averaged
only 8 trips per day to his former nest site at box 25.
The males may possibly be more active in May in establishing pos-
session of new nest sites upon their arrival from the south than they are
in preparation for second nestings in late June and July. Unfortunately,
ATTENTIVE BEHAVIOR OF THE HOUSE WREN ie
no quantitative data are available for May. However, during the first
two weeks of June there is no significant variation from the general
average for June and July.
The arrival of a new female to inspect a box and for mating purposes
is a stimulant to the male for increased activity. For instance, male
H18600 in territory 141 averaged 12 visits to his box in over 18 days, but
on June 20 a female was observed in his territory in the early morning and
there is a record of 44 trips for the day. Perhaps the female was respon-
sible for the recording of a half dozen of these trips, but the male’s excite-
ment was evidenced by increased activity at the box during the rest of
the day, after the female had gone elsewhere.
A similar record is that of the male in territory 90. From June 16 to
29, when the male was alone, he averaged 24 visits per day to this
box, but with a new female nearby the trips recorded to this box for the
insertion of more sticks averaged 125 on June 30 and July 1. The female
may have accounted for some of these recordings, although she did not
insert nest lining until July 2 and 3. She deserted without laying any
eggs, after which the male averaged only 5 trips to the box per day.
In territory 111, male C68252 was very actively singing on July 12
and made 148 trips to the box. The next day a female inspected the box
but did not stay. There is a registration of only 56 trips this day, and two
days. later the number dwindled to six. On July 18 a female came and
accepted him and his box, and 129 trips were made by the two birds
to the box.
The activity of bachelor males follows the general pattern of periods
of attentiveness alternating with periods of inattentiveness, although it is
not often practicable to analyze the length of these periods from the
itograph record. The males do not regularly enter the box at the begin-
ning and end of each period, and much of their activity during an atten-
tive period is away from the box. When the male is removing nest lining,
however, he often devotes his full attention, sometimes even to cessation
of singing, so that some idea of the length of his periods may be ob-
tained. The length of these attentive periods varies considerably, but the
average for six males when most active at this task is approximately 6
minutes (Table 1B) with intervening inattentive periods of 20 minutes.
One extreme in activity is the male in territory 98 having attentive periods
averaging 5.4 minutes spaced only 6.5 minutes apart. This male entered
the box 167 times during the day, or about 4 times each attentive period.
But in certain attentive periods, males may go in and out of the box
many times as often. The other extreme is shown by the male in terri-
tory 122 whose attentive periods at the box averaged only 3.7 minutes
and were nearly three-quarters of an hour apart. He doubtless had other
attentive periods devoted to singing or other activities, during which he
did not visit the box at all. Observations of three unmated males around
18 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
their nest gave an average of 7 minutes for 12 attentive periods devoted
entirely to singing, with inattentive periods averaging 6 minutes. A few
observations indicate that during an attentive period the intensity of
singing starts at a low level, rises to a maximum near the middle, then
decreases toward the end. Even when the male is disturbed, he scolds
only for intervals, between which he drops to the ground to eat.
Nest BUILDING BY THE FEMALE
When the female accepts a male and a nest site, she takes primary
responsibility for completing the nest. If the nest foundation of sticks
is not satisfactory, she will carry in more sticks, and the male will aid
her. Herschler (1919) observed a pair carrying in sticks and straw at the
rate of five to six times a minute. This joint action is rarely necessary,
as the female ordinarily begins insertion of the nest lining immedi-
ately, regardless of the size of the nest foundation, and in this the male
does not aid. Although the male may accompany the female on her trips
back and forth and may occasionally alight on the outer perch of the
box, he seldom enters the box after the female arrives, until the young
hatch. The record of the itograph during this period is primarily that
of the female. The record for box 6 in territory 63 is somewhat unusual
in showing 86 visits per day into the box, presumably by the female
alone, and 59 contacts per day on the outer perch only, perhaps prin-
cipally by the male. The data presented in Table 2 is therefore mainly
the record of the female’s activities.
The average of 13 records over a total of 29 days is 118 trips into the
box per day by the female. Observation indicates that the female usually
inserts material into the nest lining on each trip, although this is not in-
variable. Two or three days are normally involved in this task, but
sometimes nest lining continues to be added during egg-laying. The
average rate of trips per day, from the insertion of the first lining to the
laying of the first egg, does not give the true picture of the female's
behavior as there is a progressive change in rate from day to day. The
record for the female in territory 112 is more representative. The num-
ber of trips per day varied over four days as follows: 165, 133, 33, 47.
The nest lining was virtually completed during the first two days after
mating was consummated, after which there was a period of comparative
rest until the first egg was laid. The figures given for the maximum
number of visits per day (average maximum: 170) more nearly indicates
the rate during actual nest building, and this at times may exceed 300
trips per day. The data on minimum number of visits per day (average
minimum: 68) are usually for the interval between the near completion
of the nest lining and the laying of the first egg.
Periods of attentiveness and inattentiveness are sometimes evident in
ATTENTIVE BEHAVIOR OF THE HOUSE WREN 19
the records, but the female may not spend her entire attentive periods at
nest building and doubtless may often not visit the box at all during
periods of time between active feeding, so the data in this regard are
not satisfactory. In two records where an attempt was made to measure
the attentive periods they averaged 6.9 and 9.4 minutes, with long inter-
TABLE 2. Nest building by the female.
Number of trips
per day into box
nN
m
ee :
g <2 a 2 6 E E
= aoe m = Pet oO = =)
es é ¢ = = a aa & &
=I BS FI = 4 B S 3 z iS
3 65 ® ® Se) bs 5 > — am
ea) Ze va H ea) fy Z < = =
A94248 N 1927 63 6 June 20 2 86 98 15
B5640 R 1931 112 80A July 4 4 94 165 33
B45348 N 1928 78 51 June 27 1 104
B45348 R 1929 90 9 July 3 1 184
C68253 N 1930 96 25 June 13 76 107 44
Unknown... ——:1930 98 51 July 11 132 Roe: or
Unknown .... 1931 111 74 July 18 80 129 17
C94219 R 1932 120 53 June 5 75 97 52
Unknown .... 1931 123 10 July 19 80 65
124101 R 1934 146 49 June 23 197 294 126
207 276 138
73 116 49
159 336 83
L24987 N 1934 140 10 June 22
34-4445 N 1935 154 25 July 4
35-13635 N 1936 164 49 May 27
dow bv ww bv wre bk
J
bw
vals between. When the bird is very active, however, as the female in
territory 164 on May 27, her attentive periods averaged 7 minutes and
her inattentive periods only 10 minutes. The next day, with most of the
lining in, her attentive periods averaged 15.2 minutes and the inter-
vening periods 44.5 minutes. Probably the record obtained for this fe-
male on May 27 represents approximately the true proportions of these
periods during the active nest building phase.
THe Ecc-Layinc PERIOD
During the period of forming the set with the laying of one egg each
day, the true incubation behavior becomes established. The development
of this behavior is a gradual one with progressive changes from day
to day, so that averages and comparison of data from different females
can be made only for the corresponding days. The egg is usually laid
during the first or second attentive period after leaving the box in the
20 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
morning — not just before leaving the nest in the morning as is the case
in the great tit, Parus major ( Kluijver 1950).
House wrens lay sets varying in size from three to nine eggs, but five-
or six-egg sets are the most numerous. Elsewhere (Kendeigh 1941b) we
found that high air temperatures inhibit the laying of large sets while
low temperatures stimulate it. Air temperatures for the period 48 to 24
hours before the egg is to be laid appeared critical as to whether or not
the egg appeared—this being the presumed period of rapid increase in
size of the egg cell, just preceding passage from the ovary into the
oviduct. To determine if there were any behavior factors associated with
these environmental-physiological relations affecting the size of the egg
set, separate analyses were made of activity associated with five-egg,
six-egg, and seven-egg sets.
After the formation of a nest cavity and the laying of eggs, the thermo-
couple and potentiometer may be used. Several such records were ob-
tained which have the special advantage of showing the exact time that
the female spent on the eggs, which is, of course, of importance to their
incubation. At three nests, the temperature-recorder and itograph were
run simultaneously: A94248, C68253, C94219. A comparison of these
records shows that the female made several trips into the box each day
without sitting on the eggs. These trips were of brief duration, so the
average duration of the attentive periods as registered by the itograph
was shorter than that registered by the temperature-recorder. Likewise,
with more trips recorded, the inattentive periods were also of shorter
length.
Table 3 was compiled with the above considerations in mind. An
average of fragmentary data on seven nests with five-egg sets obtained
with the itograph shows, except for the single record for the first day,
a progressive increase in number of attentive periods per day, an increase
in their length, and a progressive decrease in the length of the intervals
away from the box. The attentive periods are similar in length as during
the nest-building period until the time the fourth egg is laid, and then
they become scmewhat longer, averaging 11.9 minutes for the last day.
It is quite possible that the periods spent away from the box are broken
up by short nonfeeding periods corresponding to periods of attentive-
ness, so they do not represent inattentive periods in the true sense. The
data show clearly that the amount of time spent away from the box
decreases as the set nears completion.
The more extensive data obtained with the temperature-recorder per-
mit more detailed analysis, although the measured periods of attentive-
ness are only for the time spent on the eggs. This, however, is of special
interest in relation to the amount of heat applied to the eggs. A com-
parison of the data for the five-egg and six-egg sets is made in figure 2.
ATTENTIVE BEHAVIOR OF THE HOUSE WREN Oak
5-e99 Sers
=~ Ogg SEIS
eer NS
\
a
Periods away
from nest
Number of
periods per day
2 3 4 5
Days on which eggs were laid
Fic. 2. Comparison of attentive behavior during egg-laying between females
laying five-egg and six-egg sets.
22. PARENTAL CARE AND ITS EVOLUTION IN BIRDS
For the five-egg sets, the development of the incubating behavior is
regular and progressive as shown by increase in number and length
of attentive periods, and decrease in periods away from the nest. The
same phenomena occur with the six-egg sets, but not until after the third
egg is laid. From figure 2, it appears that beginning with the day on
which the fourth egg is laid the increase in the number of periods per
day in six-egg sets lags about a day behind the increase in five-egg sets.
The increase in the average length of the attentive period goes along at
the same rate in both set sizes, although averaging longer in duration in
the six-egg sets. In both cases the maximum length for the attentive
period, 12.7 and 15.7 minutes, respectively, is attained on the day that
the fifth egg is laid. The decrease in average length of periods away
from the nest lags in the six-egg set about two days behind the five-egg
set during the first four days, after which the lag is equivalent to one
day. Variations in average time away from the nest is a function of the
number and duration of trips or attentive periods made to the nest, and
it appears that the chief difference in behavior of the female when lay-
ing sets of five or six eggs lies in the number of attentive periods per day.
The total daylight activity of the female during egg-laying averages
nearly 16 hours. The total percentage of this time spent on the eggs in-
creases regularly from day to day when sets of five eggs are laid: 5.0,
12.3, 19.9, 32.2, 53.3. When sets of six eggs are laid, there is again evi-
dent a lag of a day in developing the same percentage of attentiveness:
10, 9.4, 12.4; 18.1, 37.8, 52.6:
It is interesting that these differences in attentive behavior begin to
show on the day that the second egg is laid but become particularly
definite on the day that the third egg is laid. This is the third 24-hour
period before the laying of the sixth egg. As mentioned above, a pre-
vious analysis showed that environmental temperature during the second
24-hour period preceding the time of laying exerts a critical influence
on whether or not the egg is laid. The present data indicates that this
critical period also includes one day earlier, although the relative im-
portance of the third compared with the second 24-hour period preced-
ing laying is not known.
This suggests that differences in behavior are associated with dif-
ferences in environmental temperatures during this critical period when
the size of the set is determined. If air temperatures are favorable, a sixth
egg completes its development and this is correlated with a lag in the
appearance of incubating behavior. On the other hand, if conditions are
not favorable for the maturing of a sixth egg, the incubating behavior
develops much faster.
The cessation of egg-laying and onset of broodiness is believed to be
under hormonal control. This hormone may be prolactin, described by
WREN
ATTENTIVE BEHAVIOR OF THE HOUSE
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No. 4 25 23.4 12.2 29 14.9 12.6
Brooding periods decreased during the next 2 days either in number or
duration or in both. The percentage of daytime spent brooding during
the three days was 62.1, 51.7, and 20.9. In an intensive study at one nest,
Gabrielson (1913) found that the adult spent 80 to 32 per cent of her
time brooding the young throughout the period of their stay in the nest.
However, a good share of this time was protecting the young from the
intense solar radiation, and there was also an exceptional amount of
heavy rain which required the parent to protect the young from getting
wet. Gabrielson recorded a long, unbroken brooding period of 80 min-
utes and another of 180 minutes.
Of 12 records obtained by us, 10 days elapsed in eight instances and
11 days in three instances from the time the first young hatched to the
time that the first young left the nest. In addition, there are two rec-
ords of young leaving, probably prematurely, on the seventh and eighth
days, and there is one record of a single young bird that remained 15
days in the nest.
A record of feeding the young was obtained at one nest. Two young
hatched on July 25, and the third on July 26. Hardware cloth was
placed partly around the nest on this latter date, but the itograph con-
nections were not completed until July 29. With the young 5 to 11 days
old, the rate of daily feeding varied 147, 113, 187, 136, 173, 130, 195,
and averaged 147 times per day or 49 times per bird per day. The rate
was fairly uniform from day to day. Although both adults share the duty
of feeding the young, the relative amount of work performed by the
two sexes is not known in this case. At two nests that Gabrielson had
under observation at nearly all hours for a total of 12 days, the average
daily rate per bird was 32. Gabrielson found that on 8.7 per cent of the
trips to the nest, two young were fed instead of one.
Figure 27 shows the daily rhythm in various activities of the catbird
during its nesting life. The average curve for incubation behavior at
medium temperatures is for 8 days—two records from each of the four
PARENTAL CARE AND ITS EVOLUTION IN BIRDS
—
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Time of day
Fic. 27. Daily rhythm in attentive behavior of catbirds.
birds—and it shows a decrease in attentiveness until 0900 hours, a fairly
uniform rate until 1700 hours, and a rise again in the evening. At the
somewhat lower temperature of 62° F. (16.7°C.), an average of 2
days’ records shows slightly more attentiveness. At the considerably
higher temperature of 80° F. (26.7° C.), an average, again of 2 days’
records, shows a great drop in amount of time spent on the eggs, es-
pecially in the early afternoon.
The curve for the first full day of brooding, an average of records for
two different females, shows a pronounced decrease during the after-
noon when air temperatures rose. In one record for the second day
there was no brooding at all from 0900 to 1700 hours, although the av-
erage air temperature was only 72° F. (22.2°C.). The same behavior
was evident also in the incomplete record of the following day. This
daily brooding rhythm agrees, except for the exact times involved, with
the manner in which Gabrielson divided the day into three parts: the
first from 0430 to 0730 hours when the adult brooded the young to keep
them from chilling, the second from 1030 to 1400 hours when she stood
over them with outstretched wings to protect them from the heat of the
sun, and the third from 1830 hours until dark to protect them from the
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 125
chill of the evening. Although nests are ordinarily located in dense shrubs,
they are frequently exposed to the direct sun at certain hours of the
day. The shading of the young by the parents would not be registered
by our recording instruments.
The curve showing the feeding rate during the day is an average of
the last 7 days for three young in the nest. This shows a depressed rate
of feeding from 1300 to 1700 hours, the hottest hours of the day.
The females at the four nests were very irregular in the time that they
began and_ended their daily activities during incubation (Table 26).
The average of the records for the four birds gives the beginning of ac-
tivities | minute after sunrise (about 0500 hours) and their cessation 7
minutes after sunset (about 2000 hours). Allard (1930) recorded the
first singing of several male catbirds about 30 minutes before sunrise
during June and July.
The recording instrument showed that the female at nest No. 1 was
somewhat restless at night during incubation from the time that she
settled on the nest until about 0100 hour the next morning and sometimes
again from about an hour before she left the nest to begin her day’s
activity. At nest No. 3 the female was uniformly quiet all night. At nest
No. 4 the female showed slight movements all night, although somewhat
more frequently before than after midnight.
AMERICAN Rosin, Turdus migratorius
The nesting behavior of the robin has been most intensively studied
by Schantz (1939) and Howell (1942), and summarized by W. M.
Tyler (Bent 1949). Electrical apparatus was used by Schantz “to an-
nounce and record the arrivals at the two nests so that it was impossible
for the adults to come to the nest without ringing an electric bell or mak-
ing a recording on paper tape.” Both he and Howell spent many hours
in observation at the nest, and Howell has summarized the literature to
date on many phases of the bird’s behavior. Our own records of atten-
tive behavior were obtained with thermocouple and potentiometer until
the eggs hatched, after which the itograph was used at one nest.
Building of the first nest requires 5 or 6 days, but later nests may be
completed in 2 or 3 days. The work is done almost entirely by the female.
During this period the attentiveness of different males varies between
nearly complete ignorance, accompanying the female back and _ forth,
and bringing material for the female to incorporate into the nest struc-
ture. In one such latter case, Kelly (1913) reported the male making 86
and the female 108 trips to the nest during 11 hours of observation.
Schantz found that 5 days in one case and 3 days in another elapsed
between the completion of the nest and laying of the first egg. During
these intervals neither adult visited the nest more than once or twice
126 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
TABLE 28. Daily record of attentive behavior in female robins.
3 5 5 % a 5
a2 soe A =a Lo By > =
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od -'S =. o.o¢ 20h Ss £.° o°Se $O¢
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iz < 6. Za oe ie ae < 6. Zo, aS Se anon:
2nd Day (Egg-laying) 3rd Day (Egg-laying)
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3 52 12 Pes 20.1 (Deserted)
4
5
1st Day (Incubation) 2nd Day (Incubation)
2 55 33 19.7 8.1 53 27 18.6 6.3
3
5 80 37 18.0 el 82 37 17.0 8.5
3rd Day 4th Day
2 56 28 23.8 6.9 58 36 19.2 6.4
3
5 84 60 8.5 122 78 53 10.9 6.9
5th Day 6th Day
1 ae ae =o fe. 54 27 24.8 7.4
2 64. 31 20.6 8.7 58 30 2325 6.4
3
5 82 55 9.8 6.9 78 34 20.5 6.3
7th Day Sth Day
1 60 25 26.1 8.3 58 24 30.6 5.8
2, 52 30 25.35 6:2
3
5 70 30 25.6 ie. "2 59 10.2 5Lo
Sth Day 10th Day
1 54 22 32.9 6.3 oe = iy
2 56 30 PRET) 4.2 58 32 22.9 5.1
4 66 4] 16.6 6.2 79 4] 14.2 8.6
5 69 38 16.8 ThA 69 50 12.9 5v4
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 127
TABLE 28 (cont.). Daily record of attentive behavior in female robins.
ee = 6 9 =
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2 15 59 1.8 he 4.9 DIO —27 +50
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a2 The time that the daily activity began and ended in respect to sunrise and sunset is indicated
by + if after and by — if before.
> Young left nest prematurely, due to disturbance.
small spruce, an unusual location. To get the recording of an itograph
at this nest, a piece of hardware cloth was placed around back of the
nest, 6 days before hatching. The next day a tunnel, open at the top, was
made on the front side. Two days later a stake was driven into the
ground so that the top was level with the bottom of this tunnel. The
following day the itograph perches were fastened on top of this stake
and wires run to it. The next day, the recorder and batteries were con-
nected and the record started. Probably greater care and time was taken
to get the apparatus established than was necessary, but since the hermit
thrush is supposedly a shy bird around its nest, the adults were per-
mitted ample time to get adjusted to each step in the procedure before
the next one was taken. No record of incubating behavior was made.
On July 23, at least two of the three eggs hatched, and the top of the
tunnel was covered with more hardware cloth; the third young was
found hatched on July 24. The three young left before 0650 hours on
August 4 after 12 days in the nest. The record of the adult in caring for
the young is given in Table 33. Observations indicated that only one
bird, probably the female, was active in feeding the young, but of this
there could be no certainty.
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 139
There are three other records of observations at nests of this species.
In each case both adults took part in feeding the young. In McClintock’s
(1910) nest there were three young and from 89 to 205 minutes were
spent each day in watching. Stoner’s (1920) nest had four young and
from 121 to 498 minutes daily were devoted to observations. These rec-
ords are incorporated in Table 33. In a nest observed by Perry (1918),
three young were fed six times per hour on the average and left the nest
when 12 days old.
Brooding mostly ceased when the young were 3 or 4 days old, although
there may have been one short period on the sixth day. Rain fell on the
day that the young were 3 days old, which may account for the longer
brooding periods then. McClintock found the female brooding a little
on the sixth day, but Stoner does not record any brooding after the
fourth day.
The hourly rate of feeding was greater in the latter half of the nest
life than in the first half although the day-to-day increase was irregular.
The data obtained by Stoner do not show any such increase in rate
of feeding. Stoner’s data are’ unusual also in the very low rate of
feeding attained. For the seventh, eighth, and ninth days, the adults at
Kendeigh’s nest and McClintock’s nest fed their young at the average
rates of 3.5 and 3.8 times per bird per hour, respectively, but at Stoner’s
nest the adults fed four young only 1.4 times per bird per hour. Stoner
found that in 161 visits to the nest, the male and female shared nearly
alike or 82 and 79 times, respectively. He likewise observed that from
one to all four young were fed on each trip to the nest for an average of
1.5 young per visit, and that this did not vary significantly as the young
got older.
The curve (Fig. 29), showing average number of feedings at Ken-
deigh’s nest for the various hours of the day, is based on the complete
records for only the second, sixth, tenth, and eleventh days and exhibits
considerable irregularity. However, there appears a progressive decline
in the rate of feeding during the afternoon except for peaks at 1500 and
1900 hours.
The female sat on the nest every night until the young left with no
apparent uneasiness. She left the nest, on the average, 31 minutes before
sunrise, which came about 0444 hours, and returned for her next night’s
stay 35 minutes after sunset, which came about 1918 hours. Wright
(1913) states that the male’s first song comes 53 minutes before sunrise,
although he may start calling five minutes or more earlier. Thus the male
begins his activities earlier than the female; but in the evening, the last
song and call of the male averages 33 minutes after sunset which is
almost identical to the time recorded for the female to retire.
140 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
BLUEBIRD, Sialia sialis
Nearly all of the nest building of the bluebird is performed by the fe-
male and requires from 4 to 12 days. Occasionally the male may partici-
pate. Two or three days elapse between completion of the nest and laying
the first egg, according to W. P. Smith (1937b), or one week, accord-
ing to Thomas (1946). This interval, according to our records, is quite
variable and at five nests was 1, 4, 4, 5, and 8 days.
Smith gives the time of egg-laying as before 0600, between 0630 and
0800, and once at 0900 hours. We have one record of egg-laying between
0730 and 0830, another between 1000 and 1600, a third between late after-
noon one day and 0530 hours the next, but most egg-laying, not other-
wise timed, appeared to occur in the early morning. Three to six eggs
make up the set.
Smith lists two sets requiring 13 days incubation, four sets 14 days,
three sets 15 days, and two sets 16 days. Thomas gives the incubation
period as 13 to 15 days, commonly 14. The intervals between the last
egg laid and the last to hatch in three nests observed by Brodrick
(1938) were 13, 14, and 15 days. The similar interval in 11 nests ob-
served by ourselves was 14 days in all instances. In five cases the eggs
all hatched the same day; in six cases hatching extended over 2 days.
Smith states that the young generally remain in the nest for 18 days, but
he gives one instance of 17 days. Brodrick’s young birds left at 17, 18,
and 19 days after the first one hatched. Records at 10 nests studied by
us give this interval at 17 days in five cases and 18 days in the other five.
Recordings of attentive behavior are not available for the egg-laying
period, but in view of the relatively long incubation period and that all
eggs frequently hatch on the same day, it is doubtful if the first eggs
laid get very much incubation before the last one is laid.
There is no question but that the female is responsible for incubating
the eggs, although the male may be more or less attentive. W. P. Smith
(1937b), Brodrick (1938), and Laskey (1939) all give instances where
the male appeared to share this duty. Observation of the male’s entering
the nest box or even sitting on the eggs is not positive evidence, how-
ever, that he is applying any significant amount of heat to them. This
needs to be determined by either noting whether he has a brood patch
or measuring the egg temperature with thermocouple or other device.
Smith and Thomas observed the male feeding his mate at intervals, but
this seems not to be the general rule. Often he stands guard near the nest
while the female is inattentive.
Twelve days of recording at one nest and 2 days at another with
thermocouple and potentiometer indicate 34.4 attentive periods per day
averaging 14.1 minutes in length alternating with inattentive periods of
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 141
12.4 minutes (Table 34). This is a relatively low proportion of attentive-
ness, making up only 52.5 per cent of the daytime activity. The record
for bird No. 2, beginning 2 days after laying the last egg, suggests that
the attentive periods shorten somewhat and the inattentive periods
lengthen toward the end of the incubating period. This is probably cor-
related, however, with the higher temperatures prevailing during the
last 4 days.
Brooding of the hatched young is performed only by the female, al-
though both sexes usually share in feeding the young. One record of feed-
ing by both adults was obtained with the itograph at one nest for 10
days beginning the sixth day after the single nestling hatched. The total
times during the day that the adults visited the nest were 77, 71, 65, 100,
99, 74, 92, ..., ..., 104, 69, 76. The bird left the nest the next day. The
average is 82.7 trips per day. There was no increase in number of trips
with development of the young bird, but the one bird in the brood was
doubtless supplied with a surplus of food at all times. Nice (193la),
Wetherbee (1933), and Laskey (1939) have reported grown young of
a first brood helping to feed nestlings of a later second brood, but this
was not observed in this study.
TABLE 34. Attentive behavior of female bluebirds during incubation.
Difference from *
Number of Attentive Inattentive Mean daily Sunrise Sunset
Date periods periods periods temperature (min.) (min. )
per day (min. ) (min. ) Bi aC:
Nest No. 1, 1931
April 17 41 10.9 8.4 66 18.9 —16 —12
April 18 38 13.2 8.6 68 20.0 —14 +22
Nest No. 2, 1931
June 23 20 2d 18.1 72 2272 —15 +10
June 24 37 15.3 Ori. 66 18.9 — 6 + 1
June 25 40 14.6 9.2 67 19.4 —45 + 3
June 26 32 18.4 9.7 61 16.1 — 3 0
June 27 35 14.0 10.7 66 18.9 + 4 + 5
June 28 31 16.3 L2EL 68 20.0 + 9 = 2
June 29 34 14.9 10.9 68 20.0 +8 — 9
June 30 40 12.2 10.2 68 20.0 + 3 + 4
July 1 35 10.3 14. 72 DED +20 —17
July 2 38 9.8 13.9 76 24.4 + 1 +15
July 3 32 10.8 ViZaerds 79 26.1 + 6 +32
July 4 29 ORT 20.87 79 26.1 +8 + 9
«The time that the daily activity began and ended in respect to sunrise and sunset is indicated
by + if after and by — if before.
142 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Tips per hour
a &
©
V6
R4
60 100%
30
50
80
S
or Incubation re
Nest nal, ie la vr /
ei Gee
eee ‘Nest N0.2 Average: June £3- sly 40
gece re (h7°C)
Nest 10,2: Te, 34, 18°F / 40
(25.6°C)
“ok 05 06 07 08 09 10 If 12.8 4 15 16 17 18 19 20 2I
Time of day
SS per
8
BANWALO aul, jDjop fo 4Ua> Yay
Fic. 30. Daily rhythm in attentive behavior of bluebirds.
The daily rhythms of incubating attentiveness for the female at nest
No. 1 in April and nest No. 2 in late June and early July contrast in
showing the later beginning and earlier ending of the daytime depression
correlated with the difference in time of sunrise and sunset (Fig. 30).
The higher level of attentiveness maintained during the middle of the
day for the April bird is probably a response to the lower temperature.
Perhaps this species is more than usually sensitive to temperature change
as the three days’ average curve at 78° F. (25.6° C.) shows a drop in
attentiveness to a remarkably low level. The average maximum tempera-
ture on these three days was 85° F. (29.4° C.).
The greater attentiveness at 0600 compared with 0500 hours in the
curve for female No. 2 is identical to one at the same hour in the robin.
Of the 12 days entering into this curve, this fluctuation occurred eight
times, while on 3 days the record at 0600 hours was less than at 0500
hours, and on one day it was the same. Apparently the bird usually spends
a longer time away from the nest during the first hour after arising in
order to replenish energies used up overnight.
The number of attentive periods per hour increases from 1.1 at 0500
hours to a maximum of 2.8 at 0900 hours, after which it fluctuates between
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 143
2.1 and 2.7 until evening. The greater amount of inattentiveness during
the middle of the day is due not to any marked change in the length of
the inattentive periods but to these periods occurring more frequently.
This causes a pronounced decrease in the length of the attentive periods
or the length of time the female sits on the eggs at a stretch.
With hatching of the young and feeding by both adults, it appears
that the rate is greatest at 0700 and 0800 in the morning, perhaps after
the adults have satisfied their own hunger, and then decreases in a fluc-
tuating manner the rest of the day.
The time of beginning and ending of the day’s activities by the female
is remarkably inconsistent. The summary of all records indicates that on
the average the bird rose three minutes before sunrise, which occurred
at about 0546 in April and 0452 in late June and early July, and retired
four minutes after sunset, which occurred at about 1906 and 2001 dur-
ing the two periods. On individual days she departed widely from this
schedule.
Female No. 2 sat very closely on the eggs at night and was very quiet
at all times. Female No. 1, however, behaved quite differently. She was
very restless, stirring around on the eggs and getting up and down. Her
periods on and off the eggs at night were reminiscent of attentive and
inattentive periods during the day, although the periods on the eggs were
longer and the periods off the eggs shorter than in the daytime. The ito-
graph recording was somewhat imperfect, but the female apparently
brooded the young bird at night until 4 days before it left the nest.
Crepar Waxwinc, Bombycilla cedrorum
Both cedar waxwing adults share in nest building. Probably the female
does more of the work than the male. One or two trips per minute may be
made during the peak of the nest-building activity. From 5 to 7 days are
required before the nest is completed, although with renesting the time
may be shortened. The first egg is laid as soon as the nest is completed or
may be delayed for as long as three days. Additions to the nest lining
may be made during the egg-laying period. These observations were
made by Saunders 1911, Post 1916, W. A. O. Gross 1929, Crouch 1936,
Lea 1942, and Putnam 1949.
Putnam states that the eggs are laid between 0500 and 0800 hours.
Lea had data on 18 marked eggs and states that the incubation period
averages 11.7 days with variation from 11 to 13 days. James (1946)
gives 11 days and Saunders and Putnam, 12 days, for the incubation
period. At two of my nests the period was 12 days, at three nests it was
13 days. Gross gives 14 days and Post gives 15 days as the incubation
period for the nests they had under observation. Doubtless the incubat-
ing attentiveness develops gradually as the female is sometimes observed
144 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
sitting on the eggs before the set is complete and the hatching period ex-
tends from 1 to 3 days. Putnam found the adult incubating at night after
the third egg was laid.
Although Gross records both adults sharing incubation at one nest,
most students who have paid special attention to this species agree that
incubation is ordinarily performed entirely by the female. The male feeds
the female during incubation either on the nest or on some nearby perch.
Gross states that this feeding was at half-hour intervals, Crouch gives
it as 10 to 15 minutes, Lea observed it every 20 minutes. Putnam found
this rate to be variable between 0.4 and 1.4 feedings per hour. Crouch
found that the female left the nest to get this food from the male in in-
attentive periods of 3 to 5 or, rarely, 10 minutes.
Table 35 gives a record of attentive behavior at two nests, possibly of
the same female with successive broods, both obtained with a thermo-
couple inserted just above the eggs. At the first nest, due to hot weather,
the bird’s attentiveness during the middle of the day was so irregular
that definite periods could not be identified. Likewise at the second nest,
the bird did not incubate steadily during the attentive periods in the mid-
dle of the day, although there was less difficulty in recognizing the
limits of the periods. An average of the two nests makes the attentive
period 29.4 minutes long and the inattentive period 5 minutes. The atten-
tive periods not infrequently extended to over one hour in length, and
one period was nearly three hours. It is quite likely that during these
extra long periods the male fed the female on the nest, while at other
times she left the nest to receive the food. Putnam found the mean atten-
tive period to be 45 minutes in 402 hours of observation at 11 nests and
the inattentive period about 5.6 minutes. Apparently the percentage of
daytime that the bird is attentive to incubation varies between 85 and 89.
Only the female broods the young after hatching, but both adults
feed the young. Hatching occurred on July 4 at the first nest and on Aug-
ust 6 at the second nest. At this latter nest the number of attentive periods
on the day of hatching rose to 40, their average length dropped to 16.6
minutes while the length of the inattentive periods remained about the
same, 3.8 minutes. The bird thus spent 81 per cent of her time in atten-
tiveness which compares well with 87 per cent given by Lea for atten-
tiveness of the adults at his nest when the young were one to two days
old. Much of this time is spent in brooding. Lea records the percentage
of the time of the female at the nest when the young were 4 to 5 days
old as 59, 7 to 8 days old as 38, and 11 to 12 days old as 25. Of course,
less time is spent brooding and more time is spent in feeding the young as
they get older. Putnam states that the female broods 75 per cent of the
daylight hours during the first 5 days.
Lea found the average nestling period was 15.5 days with extreme
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 145
TABLE 35. Attentive behavior of female cedar waxwings during incubation.
Difference from *
Number of Attentive Inattentive Mean daily Sunrise Sunset
Date periods periods periods temperature (min. ) (min. )
per day (min. ) (min. ) ane °¢.
Nest No. 1, 1931
June 30 40 15.5 7.6 82 27.8 —12 +14
July 1 ape 23.0 6.1» 86 30.0 — 7 —31
July 2 oe Pappas 5.7> 83 28.3 — 7 —13
July 3 a 19.7” Arey? 76 24.4 — 5 + 7
Average 21.5 6.0 81.8 27.7 — 8 — 6
Nest No. 2, 1931
July 29 26 28.0 3.3 83 28.3 + 4 —46
July 30 24 31.5 5.0 76 24.4 — 4 —17
July 31 29 25.7 2.8 74 23.3 — 6 —43
Aug. 1 21 38.3 3.0 74 23.3 7 gee
Aug. 2 22 33.4 3.5 83 28.3 +50 + 3
Aug. 3 14 SY Gea 3.3 76 24.4 + 5 = 5
Aug. 4 16 46.7 6.3 78 25.6 — 4 — 6
Average 21.7 BY on 3.9 6.4 2034 + 5 —16
a The time that the daily activity began and ended in respect to sunrise and sunset is indicated
by + if after and by — if before.
>» Length of periods determined only in early morning and evening.
variations of 14 and 18 days. James (1946) found it to vary from 13 to
16 days at five nests and average 14.8 days. Putnam gives the nestling
period as 16 days. Two records of mine are for 17 days in the nest.
Saunders found the young usually remaining 16 or 17 days. One brood
that left in 14 days he recorded as being fed by the parents four times
per hour, while another brood that stayed for 18 days were fed only once
an hour. The usual interval of feeding was between three-quarters and
one hour. Gross recorded feeding of the young three times per hour. Post
observed feeding to be less frequent on hot than on cooler days. Lea
found a progressive increase in the rate of feeding five young with in-
creasing age. At ages of 1 to 2, 4 to 5, 7 to 8, and 11 to 12 days the adults
at one nest made 26, 33, 46, and 41 trips, with food or at the hourly rates
of 2.1, 2.7, 3.8, and 3.4. The male was not observed feeding on the
twelfth day, but he did 69 per cent of the feeding on the first day as
the female spent time in brooding. For the four days as a whole, he made
46 per cent of the trips with food. Up to.7 days of age, each of the five
young in the brood were fed on each visit; later an average of 3.5 young
were fed on each trip. At first the food was all crushed, but small whole
146 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
60 : a
ae ie. < ineubarion, June /2- 15 STF 0S. 9 6) 90
Brooding, Jéine 16-18
per hour
Yellow warbler a ae i Ye re
Cedar waxwing, bird nak, Incubation.
Ww ~~ Go
S gs S
4
Minutes
Q
SOE-—G5 0607 080910 ~C2 13 OAS 6 IT:~COSSCS BO
BAI4UALD aut Jojo, Jo JUaI ded
Fic. 31. Daily rhythm in attentive behavior of a female cedar waxwing and
a yellow warbler.
pin cherries were fed to the 4-day-old young, and whole June berries
and blueberries were fed to the young. when 7 to 8 days old. Doubtless
the slow rate of the feeding trips to the nest is due to the adult bird’s
ability to carry a large supply of food in its gullet and regurgitate it to
feed most or all the young on each trip. Putnam found that the feeding
rate by both sexes averaged between 2.4 and 3.9 times per hour while at
the nest, and that the young were fed by the parents for 7 or 8 days after
fledging.
Figure 31 shows the daily rhythm in attentive behavior at our second
nest during incubation. This is calculated from the full length of the
attentive period during the middle of the day, although large portions of
these periods were not spent actually on the eggs. If only the time on
the eggs were included, the depression of the curve in midday would be
more pronounced. In nest No. 1 only brief but frequent intervals were
recorded for the bird on the eggs as the nest temperature soared to 100°
and 102° F. (37.8° and 38.9° C.) in the heat of the sun. Lea found that
feeding of the young ceased during the middle of a very hot day, al-
though the female remained at the nest for one hour and forty minutes
to shade the 5-day-old young. Post, however, found that ordinarily the
young were fed more frequently during the middle of the day than to-
ward evening.
Bird No. 1 left the nest in early morning consistently a few minutes
before sunrise (0457 hours), and her last inattentiveness fluctuated
around sunset (2001 hours). Bird No. 2 varied considerably in the time
of beginning and ending her daily trips away from the nest, but they
also came about sunrise (0521 hours) and sunset (1943 hours). Some
of this irregularity may have been due to the male feeding her on the
nest so that there was no break in her attentiveness to the eggs. At both
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 147
nests the female sat very quietly at night, although at the earlier nest
the record shows the female was quite restless the night of July 3. This
may have been due to her young starting the hatching process, since
they appeared the next day. Wright (1913) has recorded the male’s first
notes one minute after sunrise and his last notes seven minutes before
sunset, so it appears that in this species the two sexes are well coordi-
nated in the time of beginning and ending of their daily activities.
YELLOW WARBLER, Dendroica petechia (aestiva)
The nesting behavior of the yellow warbler may be pieced together
from the writings of Bigglestone (1913), Mousley (1926), W. P. Smith
(1943), Schrantz (1943), and the present investigation.
Smith and Schrantz agree that only the female builds the nest, although
the male remains nearby singing at intervals. In about three hours obser-
vation during active building, the female brought material to the nest
approximately 10 times per hour. Schrantz observed at three nests that
4 days elapsed between the beginning of nest construction and the lay-
ing of the first egg, but at another nest 5 days intervened between the
completion of the nest and the first egg. Smith states that 3 to 5 days are
required for nest building and 2 more days elapse before the first egg
appears. Normally four eggs occur in a set with variations from two to
six. A day is frequently skipped in the egg-laying process. The time of
laying is between 0400 and 0500 hours in the morning. Only the female
is known to incubate.
Smith states that incubation begins with the laying of the third egg
in four-egg sets, but in one set of six, steady incubation did not begin
until the last egg appeared. We were successful in_recording attentive
behavior at one nest with the use of a thermocouple from late on the day
the second of a four-egg set was laid, June 3, 1927, until after all had
hatched (Table 36). The female sat on the eggs throughout every night
from the laying of the second egg until all hatched. The nesting was dis-
turbed on the day the second egg was laid, by the setting up of the rec-
ording equipment, but incubation was under way the next day when the
third egg appeared. The exact time of appearance of the fourth egg is
uncertain but was probably the following day. The fact that incubation
behavior begins before the last egg is laid is further shown by two eggs
hatching on June 16, one on June 17, and one on June 18. This makes
the incubation period 13 days, which is exceptionally long. At another
nest it was only 11 days. Bigglestone and Schrantz give the average incu-
bation period as 11 days, but Smith found the interval between the last
egg laid to the last one to hatch as only 10 days at three nests. |
The male feeds the female on the nest during incubation and because
of this, her attentive behavior is somewhat modified. In 4.5 hours obser-
148 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
TABLE 36. Attentive behavior of a female yellow warbler.
Difference from *
Number of Attentive Inattentive Mean daily Sunrise Sunset
Date periods periods periods temperature (min.) (min. )
per day (min.) (min.) alae at OF
1927 Egg-laying
June 4 27 23.7 5.6 66 18.9 +51 +11
June 5 eG a Seas 58 14.4
Incubation
June 6 18 34.9 Dell 52 11.1 +21 — 23
June 7 (Periods not differentiated) 59 15.0 +56 —12
June 8 (Periods not differentiated) 67 19.4 + 8 + 3
June 9 (Periods not differentiated) 73 22.8 + 7 +18
June 10 18 43.2 Ban 70 21.1: +16 +11
June 11 PA 33.2 3.3 65 18.3 — 3 —15
June 12 21 26.7 3.4 56 13.3 — 3 —3l1
June 13 18 37.9 3.2 57 13.9 +22 — 20
June 14 24 30.1 2.9 58 14.4 + 7 —43
June 15 20 44.1 D5 58 14.4 — 7 +22
Brooding
June 16 29 25.3 3.8 56 13.3 — 3 =" dl
June 17 32 22.0 5.5 60 15.6 +17 — 5
June 18 32 20.8 ul 58 14.4 +9 — 2
2 The time that the daily activity began and ended in respect to sunrise and sunset is indicated
by + if after and by — if before.
vation scattered over 7 days at our nest, this feeding of the female was
at the rate of 5.6 times per hour.
Schrantz does not present his statistical data but simply states that the
female left the eggs at intervals of fifteen to twenty minutes, presum-
ably for feeding. At our nest (Table 36), during 7 of the 10 days, the
average number of attentive periods per day was 20, their average
length, 35.7 minutes, the percentage of time attentive, 91.9, and the
inattentive periods, 3.0 minutes. The female exhibited considerable un-
easiness during her periods on the eggs and may have been annoyed by
the thermocouple across the top of the eggs. This getting up and down
and stirring on the nest may have cooled the eggs and since air tempera-
tures were considerably below normal, this may explain the unusually
long incubation of 13 days already noted. However, at night she sat
fairly quiet in spite of the thermocouple and her skin temperature was
always quite high. The unusually long attentive periods are doubtless
due to the male’s feeding her so that she did not need to leave so fre-
quently to get food. It will be noticed that her attentive periods were
shorter, but more frequent, and her inattentive periods somewhat longer
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 149
before the set of eggs was completed. During her inattentive periods the
female often did not go far away, sometimes feeding in the same tree in
which her nest was located.
On June 7, 8, and 9 it is not possible to recognize more than two or
three inattentive periods each day and these occurred after 1700 hours.
The bird exhibited her usual restlessness on the nest and may have
secured food from the tree or immediate vicinity during periods too
short to register as inattentiveness on the record. About 1°s hours of
observation on these days did not indicate that the male was feeding her
more frequently than usual. The only correlation to be made is with a
rapidly rising air temperature from the minimum of 52° F. (11.1° C.) on
June 6, to the maximum for the entire incubation period of 73° F.
(22.8° C.) on June 9. Perhaps with the rise in temperature, there was a
decrease in physiological requirement for food compared with the de-
mand at lower temperatures when metabolism becomes increased.
With the hatching of the young, the number of attentive periods per
day rose to an average of 31, their length decreased to 22.7 minutes, and
the length of the inattentive periods rose to 4.8. Brooding required 82.2
per cent of the daytime. I did not observe the male to feed the female
while she brooded, which agrees with Schrantz’s experience. Bigglestone
and Schrantz observed the male passing food to the brooding female who
then fed the young, or the male fed the young directly. Bigglestone ob-
served considerable variation in the length of brooding periods, which
generally varied between 1 minute and 10 or 12, and sometimes was
longer. After the fifth day, brooding greatly decreased. Mousley gives the
average length of the brooding period as 6.2 minutes. The longer atten-
tive periods observed by us were computed from the recording. During
these periods, brooding was frequently interrupted, and during these
times the female may have left the nest. These interruptions were never
as long as those designated as inattentive periods, but if they were
so considered, the attentive periods would probably be as short as those
observed by Bigglestone and Mousley.
The number of days that the young remain in the nest after hatching
varies between the different individuals since their hatching may ex-
tend over three days. The most common interval is 10 days after the first
hatching, at which time the last young hatched may be only 8 days old.
Schrantz found that large broods sometimes left earlier than small broods
because the crowding made them more restless.
Mousley spent 29 hours in observation of adults feeding young in the
nest at various stages in their development. During this time the young
were fed 112 times by the male and 277 times by the female or at the
rate of 13.4 times per hour. If five young remained in the nest throughout
this period, the average feeding rate per bird per hour would be 2.7.
150 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Bigglestone’s record of feeding young is most complete and detailed.
Until the young were 4 days old, the male fed them more frequently than
the female, doubtless because she spent considerable time in brooding.
The average rate of feeding of the three young during the first 6 days
was 16 times per hour. On the seventh day there was a disturbance at
the nest after which the male no longer took part in feeding the young.
During the following 4 days, the female by herself maintained the aver-
age rate of 16 times per hour, although during the 2 days preceding the
male’s desertion of his duties, her feeding rate had been only about 7
times per hour. In nearly 145 hours of observation the average feeding
rate per bird per hour was approximately 6, which is over twice the rate
reported by Mousley. In both instances the young left 10 days after
hatching. Smith observed both adults caring for the young out of the
nest for at least 17 and possibly 21 days before they became independent.
Mousley found that the male, after the young hatched, sang 1,800 times
in 29 hours or at the average rate of 62 times per hour. He never found
the male singing more often than 6 times per minute over short periods.
During egg-laying and incubation and early in the morning, Smith found
the usual rate of the male’s singing to be 4 or 5 times per minute with a
maximum of 7 times per minute.
There is very little daily rhythm in the activity of the female during
incubation (Fig. 31). On cool days, contrary to what is found in other
species, she is away from the nest more than on warm days when the
male is able to keep her appetite appeased by bringing her food while
she remains on the nest. During brooding, her curve of activity is more
like that of other species, as the male no longer feeds her and she must
search for all of her food. The least amount of time is spent brooding dur-
ing mid-afternoon when the air temperatures are highest.
The time that the female begins and ends her daily activity is quite
irregular (Table 36). Doubtless some of this irregularity is due to diffi-
culty in interpreting from the record the exact time of beginning and
ending the day’s activities. An average of all the records indicates that
she first becomes active 12 minutes after sunrise (0453 hours) during
incubation and 8 minutes after sunrise while brooding the young. Like-
wise, the termination of her daily activity averages 9 minutes before
sunset (1956 hours) during incubation and 3 minutes before sunset while
brooding. The differences in time between these two phases of nesting
activity is probably not significant. Five records of the earliest morning
song of the male, obtained by F. Allen (1913), average 33 minutes be-
fore sunrise.
According to the potentiometer record, the female sat more quietly on
the nest at night than she did during the day. Yet these quiet periods sel-
dom lasted more than 10 to 20 minutes before they were interrupted by
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 151
some movement. On one or two nights, she was seldom quiet for more
than 5 or 10 minutes. The impression gained throughout this study is
that the female is quite restless in temperament.
GoLDFINCH, Spinus tristis
One fairly complete record of attentive behavior in the goldfinch was
obtained with the temperature-recorder from midway in the egg-laying
period through incubation and hatching (Table 37). The nest was found
about one-third built on July 2, but the first egg was not laid until July 17.
Each new egg was numbered as laid until the set of six was completed
on July 22. Egg No. 1 disappeared and No. 2 was slightly crushed. Egg
No. 3 hatched first on August 2, 11 days after the last egg was laid, Nos. 4
and 5 hatched on August 3, and No. 6 hatched either late on August 3 or
more probably early on August 4. This makes the incubation period 13
days long. All four young left the nest on August 16 which is 14 days
after the first one hatched. Both adults shared in feeding the young
while in the nest.
Various phases of the nesting behavior of this species have been studied
by Bruce (1898), Mousley (1930a, b, 1932, 1935), A. O. Gross (1938b ),
Walkinshaw (1938-1939), and Stokes (1950). The female does all of the
nest construction. The male is generally nearby, singing, and accom-
panies the female on her trips. He may rarely bring nest material for the
female to insert into the structure. Thirteen days are required to construct
the nest in early July but only 5.6 days in late August. Copulation is prob-
ably frequent during this period. There may be a lapse of 2 days be-
tween the completion of the nest and the laying of the first egg early in
the season but none later. The eggs are laid daily early in the morning,
although Gross found the first egg of one set to be laid between noon and
1600 hours. Five eggs is the most common number in a complete set,
although Walkinshaw gives the average of all sets as 4.5 eggs. Stokes
found the size of sets to be 5.3 in July and then to decrease to 3.7 in late
August.
All authorities agree that steady incubation begins before the set is
completed, and this is further substantiated by hatching extending over
2 or commonly 3 days. Walkinshaw (1938-39) states that in four-egg sets
the female begins incubation and is on at night for the first time after
laying the second egg, while in five-egg sets she does not do so until the
third egg is laid, but there are variations from this schedule. At the nest
which we studied, the female was observed on the nest in the morning
after the first egg was laid but not in the afternoon or at night. The fe-
male was frequently seen on the eggs in the morning after the second
egg was laid and was on twice in the afternoon, for periods of 19 minutes
each, after the thermocouple was inserted in the nest at 1530 hours.
152 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Table 37 shows that the attentive periods became longer and the inatten-
tive periods shorter with the laying of successive eggs and during the
first 3 days of incubation. The bird went on and off the eggs more
frequently at this time than when she settled down for incubation at a
slower routine. In this case the first night that the bird spent on the nest
was the night before the last egg in the set was laid, when she was fairly
quiet and applied full heat to the eggs.
Walkinshaw has the most extensive data and places the average length
of the incubation period for 33 sets at 13 days. All authorities agree that
incubation is performed entirely by the female and that the male regu-
larly feeds the female at the nest. Mousley (1935) has evidence that the
female sometimes raises a second brood in which case she does so alone,
while the male takes full responsibility for caring for the young of the
first brood after they fly and does not come at all to the female’s second
nest. Gross found that the male started feeding the female at the nest
at intervals of one-half hour as soon as incubation began during the
egg-laying period.
The attentive periods of the female during incubation are very long,
averaging 2.2 hours. Doubtless this is because the male feeds the female
at the nest. There is one record on July 29 of the female staying continu-
ously at the nest for nearly 10.5 hours and another record of 9.5 hours on
August 1. There may be some question whether the female exhibits
attentive and inattentive periods at all during incubation. However, she
does leave the nest and eggs for intervals that average 8.7 minutes which
are convenient to recognize as a vestige, at least, of inattentiveness. The
total time away from the nest during the day and night averages only
about one hour. Sitting on the eggs takes up 92 to 100 per cent of the
time. There is a little evidence that on cool days she leaves the nest more
frequently than on warm days although not for very long at a time. The
female does not sit quietly during these long attentive periods but shifts
around on the eggs, jumps back and forth to the rim of the nest, rises
up to receive food from the male, and may leave the nest entirely for
several seconds at a time while she moves around nearby.
Hatching extended over 3 days. In general, the attentive or brooding
periods are better differentiated than during incubation and they are less
than one-third as long, averaging 15.7 per day, 37.1 minutes long. Brood-
ing requires 76.5 per cent of the daytime. Inattentive periods average 10.7
minutes. The short time spent in attentiveness during these 3 days may
have partly been due, however, to the higher air temperatures that pre-
vailed. Mousley found at one nest that the brooding periods averaged
18.5 minutes during the first 7 days and at another nest they averaged
14.9 minutes. There is a progressive decrease in amount of time spent
brooding until it nearly ceases after the young are 6 or 7 days old. On
153
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154 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
hot days the female may devote her attentive period to standing on the
rim and shading the young from the direct rays of the sun rather than in
keeping them warm. During rain or cold weather the female may cover
the young at least up to 11 days of age.
When the female is brooding the young, the male continues to feed
her at the nest. Some of this food she keeps for herself, the rest she hands
over to the young. When the female is away and after brooding is over,
both male and female feed the young directly. When the female ceases
to brood, the male no longer feeds her even though she begs for it.
Feeding is by regurgitation of food previously ingested and perhaps
partly digested. This permits the adults to bring more food at a time and
to feed it at intervals. Mousley (1932) observed the female leaving the
nest twice in three hours to search for food, yet she was able to feed the
young nine times during this period. A. O. Gross (1938b) observed that
the male fed each of six young on each visit, sometimes repeating the
round more than once; however, the female fed only two to four of the
young at a time. Doubtless this manner of feeding is responsible for the
slow rate of feeding the young customary in this species.
Bruce found at one nest that the young were fed at the rate of about
once per hour by the male and female. Mousley spent over 164 hours in
observation at four different nests and found that the rates of feeding at
the different nests varied between 1.1 and 1.6 times per hour for a gen-
eral average of 1.4. The rate is no faster with both adults feeding the
young than with the female feeding them alone. At one nest the rate
of feeding tended to decrease as the young got older, but at another nest
the rate remained about the same throughout. Walkinshaw found during
10.5 hours of observation that the young were fed about twice per hour
by the male and female. Due partly to hatching being prolonged, the
young leave the nest at ages varying from 11 to 15 days, but the average
is 13 days. Both adults may continue to feed the young periodically for
several more days, or the female may start a second nest leaving the care
of the young of the first brood to the male (Mousley 1935).
Gross observed that when the construction of the nest was nearing
completion the female made her visits only in the early morning and
again one to two hours before sunset. Figure 32 shows the daily rhythm
of activity of the female at various stages in her nesting cycle as shown
by our temperature-recorder. To simplify the figure and because the rec-
ord for the third and fourth days of egg-laying are nearly the same, the
hourly data for these 2 days have been averaged together. The same was
done for the fifth and sixth days. The curve for the incubation period is
an average for 7 days and the curve for brooding is an average for 3 days.
The incubating behavior exhibits a progressive development during the
egg-laying period. On the days that the third and fourth eggs are laid
ob
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 155
Brooding
S
oS
jojo, fo *4uar sed
Incubation
S “ee , ea 20
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hemes
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” Time “of day
Fic. 32. Daily rhythm of attentiveness of female goldfinches.
attentiveness is most pronounced from 0600 to 1400 hours. On the days
that the fifth and the last eggs are laid, attentiveness is well sustained
throughout the day. With full incubating behavior established, the
curve shows a tendency to drop slightly in the late afternoon. Differences
in daily temperature produced a negligible effect during incubation, but
the pronounced drop in the curve for brooding after the middle of the
day may have been accentuated by the prevailing heat. If the female
were standing on the rim, shading the young from the sun in the after-
noon, her attentiveness would be longer than the record showed. The
various curves indicate, however, that through most of the nesting cycle
there is decreased activity in the afternoon. No data are available to show
the daily rhythm in rate of feeding.
The first inattentiveness of the female in the morning during incuba-
156 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
tion, but excluding July 21 and 22, averaged 45 minutes after sunrise
(Table 37). Sunrise occurred at about 0518 hours. This is not a true index
in this species of the commencement of the day’s activities as the female
becomes active on the nest long before this time. Gross (1938b) states
that the male makes his first visit to the nest at dawn. Actually the tem-
perature record indicates that restlessness of the female began 18 min-
utes before sunrise on all except two mornings. Probably this is the time
that the male starts feeding the female on the nest.
Gross (1938b) also states that the male continues to feed the female
at intervals well after sunset. This may well be the case, as the last in-
attentive period was completed 52 minutes before sunset (1947 hours).
On 6 evenings the female continued to be restless until 14 minutes after
sunset. On some evenings, however, there is no certainty that the male
continued to feed her until this late. While brooding the young, the
female does not leave the nest until much later in the morning but may
be off at a later time in the evening. Except for the early morning and
evening restlessness already noted, the female usually spent a quiet
night on the nest.
Curppinc Sparrow, Spizella passerina
Although several attempts at detailed studies of the chipping sparrow
were made, only once were we able to get a successful recording of nest
activity with potentiometer and thermocouple. The birds, especially the
female, seemed unusually sensitive to disturbance, and this species
proved to be one of the most difficult with which we have worked. It is
fortunate that Walkinshaw (1944) has summarized his observations so
that the nesting history of this bird may be pieced together.
According to Walkinshaw, the male sings in defense of territory almost
continuously during the daylight hours from the time of his arrival in
migration until mating is completed, but sings very little between mating
and the beginning of incubation. The female does all the nest building,
although the male usually accompanies her on her trips back and forth.
The nest is completed in 3.4 days, on the average.
The eggs are laid daily between 0500 and 0700 hours until three or
four are laid. Only the female regularly incubates the eggs, although
Walkinshaw once saw the male covering them. Only 10 days elapsed
between the last egg laid and the first young to hatch in the four nests
where this was determined. Walkinshaw found the female on the eggs
the night before the last one was laid and computes, therefore, the incu-
bation period at 11 days. At five nests of ours, 11 days (10-12 days)
elapsed between the last egg laid and the first to hatch, and since the
hatching extended over 1, 2, and even 3 days in one instance, the incuba-
tion period was more nearly 12 days long.
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 157
TABLE 38. Attentive behavior of a female chipping sparrow during incubation.
Difference from *
Number of Attentive Inattentive Mean daily Sunrise Sunset
Date periods periods periods temperature (min. ) (min. )
per. day (min. ) (min. ) °F. a OF
1931
July 16 nee ee i 82 27.8 eee aa)
July 17 38 10.3 12.3 84 28.9 + 7 —19
July 18 44 11.6 8.6 78 25.6 — 6 +10
July 19 Sse: ete aif 82 27.8 oe —15
July 20 34 Welt 8.6 78 25/6 —12 —15
July 21 32 21.8 6.2 70 201 — 20
July 22 Be cies ee 72 22.2 —22
. The time that the daily activity began and ended in respect to sunrise and sunset is indicated
by + if after and by — if before.
Table 38 summarizes one record of attentive behavior. There were
37.0 attentive periods per day, averaging 15.2 minutes in length, with the
inattentive periods 8.5 minutes long. The bird sat on the eggs 66.0 per
cent of the daytime. The table indicates a possible increase in length of
the attentive periods and decrease in length of the inattentive periods
with progress of incubation, but more probably this is correlated with
the decrease in mean daily temperature. We did not observe the male
to feed the female at the nest, but Rudolphi (1935) and Bradley (1939)
found that the male brought food about two times per hour “sometimes
feeding her while she remained on the nest and sometimes coming to a
nearby tree or bush where she met him and received the food.”
Walkinshaw found that the female did most of the brooding of the
young, but on cool mornings the male occasionally brooded for a very
few minutes. Nearly 10 hours of observation early in the morning on
the day the young hatched and the next two days showed a steady de-
crease in average length of the brooding period from 41.1 to 14.2 to 11.1
minutes with intervals between brooding increasing from 3.8 to 12.0 to
13.7 minutes. Brooding ceased entirely during the daytime after the
young were 6 or 7 days old.
Walkinshaw spent over nine hours in observation of feeding the young
at one nest and seven hours at another nest. Both nests contained three
young. At the first nest the rate of feeding increased with the age of
the young as follows: just hatched—2.0 times per hour; one to two days—
8 times per hour; and six to seven days—11.2 times per hour. At the other
nest the rate varied: one to two days—6.4 times per hour; two to three
days—6.5 times per hour; and four to five days—13.3 times per hour. Both
158 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
male and female took nearly equal parts in feeding the young. The
young left the nest when they were 7 and 8 days old, which is before
they were able to fly. F. E. L. Beal watched two nests with four young
each at ages of 4 and 6 days for 14 hours and found the adults feeding
at the rate of 19 and 17 times per hour. In five records of ours, an aver-
age of 9 days elapsed (8-10 days) between the first young to hatch and
the first to leave the nest. Walkinshaw observed the young fed by their
parents when 24, 33, and perhaps 35 or 40 days old.
Most of the nest building is done in the early morning hours. The daily
rhythm of activity during incubation as obtained by the recording poten-
tiometer is shown in figure 33. Less time is spent incubating on warm than
on cool days. On July 21 when there was rain and cool weather, the
female stayed on the eggs for one long period of 129 minutes and several
other periods of one-half to three-quarters of an hour. The record on all
4 days, regardless of the temperature, shows a secondary rise sometime
between 1000 and 1200 hours before dropping to the afternoon low.
Perhaps this was a peculiarity of this particular individual. The number of
periods per hour increases steadily from 1.5 at 0500 hours to a maximum
of 3.3 at 1500 and 1600 hours and then regresses. The length of the in-
attentive periods does not show any consistent variation with time of
day, but the attentive periods vary as follows: 0500 to 0800 hours, in-
clusive—21.8 minutes; 0900 to 1200 hours—26.4, although the average
would be 12.1 if the rainy July 21 is omitted; 1300 to 1600 hours—11.1;
1700 to 2000 hours—13.4. The relatively long brooding periods recorded
605
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Time of day
Fic. 33. Daily rhythm of attentiveness of female chipping sparrows during
incubation.
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 159
by Walkinshaw are probably to be explained by the time of day, as all
of his observations were made between 0500 and 0930 hours.
This bird showed the interesting trait of beginning her daily activities
earlier on cool than on warm mornings, although no such relation with
temperature is evident in the time her daily activities terminated in the
evening (Table 38). On the average she left the nest 11 minutes before
sunrise (0510 hours) and retired 6 minutes before sunset (1954 hours ).
Allard (1930) registered the first morning song of the male about 30
minutes before sunrise or close to 20 minutes before the female becomes
active.
The potentiometer recorded the female somewhat restless on 3 out of
5 nights. Twice the bird became more restless just before leaving the
nest in the early morning, on one occasion for one-half hour, on the other
for 15 minutes. Near midnight on July 21-22 there was a severe thunder-
storm. The bird had been quiet on her nest previously, but beginning at
0015 hours she left the eggs for two periods totalling 33 minutes. Perhaps
the eggs and nest got soaked, because when the bird returned she was
restless the rest of the night. The eggs, however, hatched successfully.
Sonc Sparrow, Melospiza melodia
The potentiometer and thermocouple were used to record the activity
of five female song sparrows over a total of 35 days during incubation
and brooding. No detailed observations were made at the nest nor of the
male’s activities. The male is chiefly responsible for the establishment and
defense of the nesting territory and helps to feed the young. The female
does all the nest building, incubation, brooding, and part of the feeding
of the young.
Singing of the male. Nice (1943:119) obtained records on the rate of
singing for eight males over 500 hours and found that the rate varied
under different conditions as follows:
Times per hour Stage of nesting cycle
0-20 Prenuptial, preliminary nest building and coition,
feeding young, molt
30-70 Building, egg-laying, incubation, late afternoon
90-160 Competitive singing between males, proclaiming ter-
ritory in summer, cold days in spring
180-300 Proclaiming territory in spring, competitive singing
between males.
One male while proclaiming territory sang 4.8 times a minute for the first
two hours in the morning with only one-half minute inattentive periods.
During the next hour he was inattentive and not singing for only 12.5
minutes. During the afternoon, however, his singing was less intense and
continuous (Fig. 35).
160 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Nest building of the female. A few observations by Nice (1943:210)
of one female during nest building gave attentive periods of 15, 20, and
23 minutes with intervening inattentive periods of 5, 7, and 8 minutes.
The nest is nearly completed within 2 days and lined by the third or
fourth day, with the first egg commonly coming on the fifth day. Nor-
mally three to five eggs occur in a set. The brood patch begins to de-
velop 4 to 6 days before the egg is laid so that with the first egg the
TaBLE 39. Daily record of attentive behavior of female song sparrows.
S o 5 i) o &
42 = = = ae) : > =
BBG RT See ge q5° 24 22 eee
rd a Zi oN ee a ee 26. “28 asec
Ist Day (Incubation) 2nd Day
Di eater
3
5 72°F 20 29.2 11.7 69°F. 20 32.0 8.8
3rd Day 4th Day
1
2
3
5 70 16 34.0 10.2
5th Day 6th Day
1 52 38 15.2 6.1
2
3
5 61 25 26.2 ee 60 27 22.2 8.6
7th Day Sth Day
i 46 35 18.5 5.3 52 29 20.1 Cet
3 hes: a ie cae 72 18 39.7 8.6
1 to 13 48.9 10.4 uae wae a ee.
i) 66 33 16.9 9.5 64 30 19.5 1.3
Ith Day 10th Day
1 43 31 22.4 4.1
2 a, a re ae 67 27 21.0 12.2
3 80 20 36.3 8.9 78 17 39.4 10.9
4 te hie Ae ae 83 15 41.1 19.5
5 68 28 21.0 8.3 77 27 20.9 9.5
ATTENTIVE BEHAVIOR OF MISCELLANEOUS: SPECIES 161
TaBLE 39 (cont.). Daily record of attentive behavior of female song sparrows.
s 2 5 n ne, MR = Nn ao S 5 vA ve Nn =| N
8 HoH Sn | eI my son fH Shs
Z aoe Z2oemte®, £55 aor so, os (S22
11th Day 12th Day
1 44°F, 32 21.0 4.5 55°F. = 33 18.4 6.6
2 68 26 26.5 7.3 66 22 32.6 7.9
3 68 23 28.7 Cee 72 17 36.2 11.1
4 84 20 32.3 14.8 78 13 47.2 Lilecl:
5 70 26 24.0 7.3 62 23 27.5 (a3
O Day (Hatching) 1st Day (Brooding)
1 56 58 9.2 5.6 52 73 7.4 4.6
2
4 83 29 16.1 16.1 73 ? 23.5 7.6
5 62 37 18.1 5.9 64 38 14.1 6.9
2nd Day
1 51 56 8.7 6.5
2
4 72 48 11.3 5.8
5 67 39 11.4 10.5
patch is entirely bare and vascularized (Nice 1937:122). Eggs are laid
in the early morning on succeeding days. The incubation period is most
often 12 or 13 days in length.
Egg-laying. Nice is correct in stating that incubation begins before
the set is complete, since normally two days are required for all the eggs
to hatch (1937:122). Only one record was obtained in the present study
during the egg-laying period. At nest No. 5 the female had six attentive
periods totaling 43 minutes from 1430 hours until dark on the day that
the first in a two-egg set was laid, compared with six attentive periods
totalling 219 minutes over the same time the next day. She did not spend
the night on the eggs on the first day, although she did thereafter
throughout incubation.
Incubation. During incubation, the attentive periods of the female
average 28.5 minutes, her inattentive periods average 8.8 minutes, and
there are 23 attentive periods per day (Table 40). Thus the bird is atten-
tive 75.6 per cent of the daytime. There is considerable variation between
different birds and with the same individual at different times. Only the
record at nest No. 5 extends throughout the incubation period (Table
162 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
39). The number and length of her periods are somewhat greater during
the first three days than later during incubation. Considering all these
records and Nice’s observations (1937:124), there is probably, however,
no consistent variation in attentive behavior with progress of incubation.
There appears to be a definite correlation between average number
and length of periods with average temperature. This correlation was also
evident when the daily records, irrespective of the individual on which
they were obtained, were considered. Since the increase in length of at-
tentive period with rise in temperature is contrary to what occurs in other
species, since it does not agree with similar data obtained by Nice, and
since it is not supported by the curves of daily rhythm on hot and cool
days (Fig. 34), the apparent correlation requires further scrutiny.
When the daily averages for individual sparrows are considered
separately, the length of the attentive periods decreases with rise in
temperature at nests No. 1 and 4, increases at nest No. 3, while at nest
No. 5 the trend is uncertain since it decreases as temperatures rise from
60° to 68° F. (15.6° to 20.0° C.) but is greatest at temperatures of 69°
TABLE 40. Attentive behavior of female song sparrows.
Incubation
Air Number Atten- Inatten- Total
Number Date of Days’ tempera- of tive tive atten-
of eggs last record ture periods periods periods _ tiveness
in set egg °F. °C. perday — (min.) (min. ) (min.)
Nest
1 4 May 6 6 49 9.4 33 19.3 Dek 637
2 4 June 8 3 67 =19.4 25 26.7 9.1 668
3 3 June 11 5 74 -23..3 19 36.1 9.3 686
4 4 July 16 4 80 26.7 15 42.4 15.6 636
5 2 July 29 11 67 19.4 25 24.9 8.7 622
Bird Data compiled from Nice, 1937, p. 123
K7 ... April 17 hours 57 13.9... 30.5 6.0
K2 oe April 380 hours 55 12.8 ee 30.0 7.8
K2 ... June 21 hours 70 21.1 mete 27.0 9.0
K3 ... June 24hours 69 20.6... 20.0 8.0
Brooding (first two days after hatching)
Air
Number Date tem- Number Brooding Intervals Total
of first perature of periods (min. ) brooding
young hatched °F. °C. periods (min. ) (min. )
Nest
1 3 May 18 52 11.1 64 8.0 5.6 512
4 3 July328. -72 -(2222 0 5. 17.4 6.7 eat
5 2 Aug. 10 66 18.9 38 12.8 8.7 486
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 163
to 72° F. (20.6° to 22.2° C.). Female No. 3 was an exceptional bird in
that high temperature appeared to make her nervous. The record shows
that during the middle of the day she would spend long periods at the
nest. One such period was three hours long, another nearly four hours
long. She did not incubate steadily. The nest temperature was in almost
continual flux as if she were hopping on and off the eggs. There was never
a period of more than three or four minutes when she was away from
the nest, but she may have picked up occasional tidbits to eat in these
intervals. As the air temperature moderated in late afternoon, her be-
havior became normal again and her attentive and inattentive periods
became typical of the species. The unusual relation between length of
attentive periods and temperature in our records for this species is appar-
ently due to the nervous idiosyncracies of one or two birds.
Further study of the daily records of individual birds showed no con-
sistent change in the number of periods per day with increase in tempera-
ture. Considerable irregularity occurred from day to day. On the other
hand, all four birds (nests 1, 3, 4, 5) showed without exception an
increase in the length of the inattentive period as the air temperature in-
creased. The daily records for all birds in each range of temperature show
that the length of the inattentive period varied: 4.6 minutes at 44° F.
(6.7° C.), 7.2 minutes at 55°F. (12.8°C.), 84 minutes at 67°F.
(19.4° C.), 11.1 minutes at 76° F. (24.4° C.), and 17.2 minutes at 84° F.
(28.9° C.). This is in harmony with the relation between inattentiveness
and temperature found in other species. The total attentive time during
the daylight hours averages nearly the same for all five birds regardless
of the temperature, so that the manner in which this time is divided be-
tween attentive and inattentive periods is peculiar to the individual.
The male may have an influence in determining the behavior of indi-
vidual females. Nice (1937:124) noted that the similarity in length of
attentive periods of K7 and K2 may be due to their being mated in differ-
ent years to the same male. She also found that the female, two-thirds of
the time, terminated her attentive period in answer to signal-songs of the
male given within 20 feet of the nest. While the female is inattentive,
the male guards the nest for a few minutes, then leaves to join his mate
and often accompanies her back. While the female is on the nest, the
male sings and has his inattentive period for feeding just before the
female is due to leave the nest.
When total attentive time per day is averaged for days with different
numbers of attentive periods, it fluctuates around a constant value of
638 minutes regardless of whether the average number of periods is 14,
18, 23, 28, or 33 per day. Likewise the total inattentive time varies around
204 minutes. The increase in number of periods per day is correlated
164 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
with a proportionate decrease in the length of both the attentive and in-
attentive periods.
Brooding young. From Table 39, it is evident that as soon as the eggs
begin to hatch there is a marked increase in number of attentive periods
per day, as measured by the time spent brooding, and a decrease in the
average length of these periods. The inattentive periods may remain of
the same length as before or may decrease. The data on brooding be-
havior are averaged for the first and second days after the one on which
the eggs hatch (Table 40), as on the day of hatching part of the time
is spent in incubating the eggs. During these two days, 64 per cent of
the time is spent in brooding the young, there are 51 brooding periods
per day, their average duration is 12.7 minutes, and the intervals be-
tween brooding periods average 7.0 minutes. For the corresponding two
days Nice (1937:130) records the female brooding only 52 per cent of
60; 1/00 %
90
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04-05 06 07 08 09 lO_if l2 13/4 I5 16 17 (619° 2002]
Time of day
Fic. 34. Daily rhythm in attentiveness of female song sparrows during in-
cubation.
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 165
&
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Time of day
Fic. 35. Daily rhythm in attentive behavior of song sparrows.
the time, but her observations probably did not include the early morn-
ing and the evening when a greater proportion of time is devoted to this
activity. She found, however, that a similar proportion of time spent
brooding persisted into the third or fourth day, and then dwindled to
almost none after the sixth day. The young stay in the nest for 10 days
and are cared for after leaving for another 18 to 20 days.
Feeding young. No records were made in the present investigation on
the rate of feeding the young. Nice (1943:231) has summarized her
own observations and those of Haldeman and Mousley. For the first
5 days of nest life the young are fed, on an average, 7.2 times per hour,
5.2 times by the male and 2.0 times by the female. During the second
5-day period they are fed 17.8 times per hour, 9.7 times by the male and
8.3 times by the female. At three out of five nests during the second period
the females fed more frequently than the males since they did not then
need to devote time to brooding. The rate of feeding by both adults was
2.5 times more rapid during the second 5 days than during the first 5
days, corresponding to the increased requirements of the young as they
grew older. The average rate for the entire nesting period, obtained by
averaging the two rates given above, is 12.5 times per hour. As there
was an average of 3.7 young per nest, the number of trips to the nest
was at the rate of 3.4 per young bird per hour. Haldeman (1931:399 )
found that when the young were approximately 5 days old an average
of 1.4 young were fed on each visit by the parents to the nest, but there
166 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
is no information available whether this rate is maintained throughout
the nest life. In one all-day record, Copeland (1909) found an average
rate of only 5.5 feedings per hour.
Daily rhythm. Nice (1943:122) recorded the number of times an eight-
to nine-year-old male sang each hour throughout the day when pro-
claiming territory and seeking a mate. Her data are plotted in figure 35
and they show that he was most actively singing early in the morning, at
a slightly decreasing rate until 1300 hours, and then at a considerably
decreased rate the rest of the day. There was no resurgence of active
singing in the evening.
The daily rhythm of incubating activity is shown for three birds in
figure 34, both for warm and cool days. The greater depression of atten-
tiveness on hot days is evident for females No. | and 5, and the peculiar
behavior of female No. 3 has already been mentioned (p. 163). An aver-
age curve for all five females under various conditions of weather shows
a constant level of attentiveness from 0800 to 1800 hours. There were no
consistent changes during these hours in number of periods nor in length
of the attentive and inattentive periods.
A record of two females brooding over 4 days (Fig. 35) shows a typical
curve of decreasing time spent on the young until noon, a continuance of
brooding for only 30 to 35 minutes during each hour until 1800 hours,
and then an increasing amount again in the evening.
The curve for hourly feeding rate is taken from Haldeman (1931:396 )
and is for young which she estimated to be in their fifth day after hatch-
ing but which Nice (1943:231) believed may have been 6 or 7 days
old. Haldeman found that the female fed at a rapid but decreasing rate
all morning and at a slow rate in the afternoon. The rate of feeding by
the male was the reverse, and during two hours in the afternoon he fed
the young more often than did the female. Of the total feedings during
the day, the female gave 198, the male, 63.
Beginning and ending of day’s activities. In considering time of be-
ginning and ending of the birds’ daily activities, it is again necessary to
separate the various phases of the nesting cycle. When caring for young
birds in the nest, the female arises 28 minutes earlier and retires 9 min-
utes later than when incubating eggs (Table 41).
During incubation the female first leaves the nest after a night on the
eggs at 2 minutes, on the average, after sunrise and returns to the nest
in the evening 5 minutes before sunset. While brooding she anticipates
sunrise fully 26 minutes and retires 4 minutes after sunset. There is con-
siderable variation between different females and in the same female
on different days. Arising late and retiring early is the rule on cloudy
and rainy days, but the necessary data are not at hand to analyze this
modification of behavior in detail.
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 167
Nice (1943:101, 107) obtained 11 records on three females and found
that they arose 23 to 25 minutes before sunrise and retired about sunset.
She does not state the nesting activity of the birds at the time, but the
records would agree with ours for the period after the young hatch.
Allard (1930:440) and Nice (1943:102) agree that during the breeding
season the males begin singing about a half-hour before sunrise and Nice
(1943:107) finds that he does not go to roost until 14 minutes after sun-
set. Cloudiness shortened the day’s activity at both ends. Wright (1913),
on the other hand, recorded the male’s first song an average of 73 min-
utes before sunrise and his last song 23 minutes after sunset.
TABLE 41. Time of beginning and ending of daily activity in female song sparrows.
Number of records Difference from
Median Hour Hour
Nest date Morning Evening activity activity Sunrise Sunset
began ended (min. ) (min. )
Incubating eggs
1 May 14 6 7 0530 1917 +19 —17
2 June 17 4 4 0455 2000 + 2 +]
3 June 20 6 5 0452 1944 — 2 —16
4 July 25 6 5 0504 2015 —10 +25
5 Aug. 4 11 12 0523 1920 — 1 — 20
Brooding and feeding young
1 May 18 3 3 0444 1929 —22 — 9
2 June 19 — 1 ae 1957 an —:
4 July 29 1 2 0445 2002 —33 +16
5 Aug. 11 2 3 0507 1944 — 23 +13
Activity a night. The temperature record shows that at nests 4 and 5
the females were usually fairly quiet all night long, although in the early
part of the night of July 31, the female at No. 5 left her eggs. From 2040
to 2125 hours she was probably perched on the nest rim as the thermo-
couple recorded some heat, but from 2125 to 2300 hours she was away
from the nest entirely. After 2300 hours she settled down on the eggs
for the rest of the night. The female at nest No. 3 was very restless at
night, but this may have been due to the experimental use of two thermo-
couples in the nest instead of one. Females Nos. 1 and 2 showed some
restlessness at more or less definite intervals of 15 to 30 minutes and 10
to 20 minutes, respectively. No bird showed any consistently greater
restlessness at one hour of the night than another. Females Nos. 1 and 5
were considerably more restless the first 2 or 3 nights after the young
hatched than they were when incubating eggs.
168 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
DISCUSSION AND SUMMARY
The analysis of attentive behavior in different species indicates that
considerable variation occurs. The general rule is for both sexes to share
nesting duties but in greatly varying proportions. In species having a low
taxonomic position, such as killdeer, chimney swift, and flicker, both
sexes share incubation as well as the care of the young. In species of
more advanced ranking, the male commonly does not incubate or brood,
but he helps to feed the young. In some species, as the cedar waxwing,
yellow warbler, and goldfinch, the male has not only lost the incubating
behavior but has developed a new trait of keeping the incubating fe-
male supplied with food so that she seldom needs to leave the nest and
search for food for herself.
Coincident with the loss of incubating behavior in the male has been
the loss of a brood patch, such as the female retains and such as males
of the lower orders also possess. Without a brood patch the male does
not truly incubate even if he sits on the eggs during the female's ab-
sence. In addition to instances noted for some of the above species,
Ryves (1943a) cites several others where the male may “sit on eggs with-
out the production of the requisite temperature to further their develop-
ment,” and he also points out that this behavior on the part of the male
should not be considered true incubation. He proposes that this male
behavior be called “brooding,” but we prefer to limit this term to the ap-
plication of heat to young birds after hatching.
There are several other important variations between species in atten-
tive behavior, but the analysis and interpretation of these various types
of behavior patterns will be postponed to the next section.
A common characteristic of all behavior patterns is the gradual way
in which they develop and then recede during the yearly reproductive
cycle. The earlier recrudescence of reproductive behavior in the male
than the female is doubtless conditioned by the earlier development of
the testes in response to the lengthening photoperiods of early spring.
After migration is completed, the male then establishes his territory and
may start nest construction. When the female arrives and mating is
consummated, nest building proceeds in earnest, followed by egg-laying
and onset of incubation. Reproductive behavior undoubtedly depends on
hormones liberated from the maturing gonads and may also require
stimulation from the opposite sex as well as a proper environment. After
reproduction has run its full course, there is regression again to the
quiescent winter condition. This is also a gradual process with the male,
and he usually precedes the female in returning to the nonbreeding con-
dition. This gradual retrogression occurs along with the atrophying of
the gonads and the progressive gaining of independence by the young.
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES 169
Doubtless the time will come when it will be known how each stage in
this cycle is controlled and coordinated with all the other stages and the
relative roles played in this regulatory mechanism by hormones, weather,
companions, energy resources, and other factors. It may well be that each
stage in the reproductive cycle serves as the stimulus to initiate the next,
as Herrick (1910b) maintained long ago.
Nest building commonly proceeds vigorously from the very start,
once the female and male have definitely become mated. Usually the nest
is essentially completed sometime before the female is ready to lay
her first egg. As a result the nest may not be visited during this interim
of one or more days and attentive behavior may appear at low ebb. In
passerine species, 5 or more days may elapse between first copulations be-
tween sexes and the laying of the first egg. Usually not all of this time is
required for nest building.
Considerable evidence has been presented in this paper that incubation
attentiveness develops gradually. Ryves (1943a) discussed the problem
several years ago and Swanberg (1950) more recently. Purchon (1948)
showed that as the four eggs were laid, a female Hirundo rustica spent
daily increasing percentages of time on the nest: 16.7, 20.1, 45.0, and
58.1. Only on the last day did the average length of the attentive period
exceed the inattentive period. In the avocet, Recurvirostra avosetta,
P. E. Brown (1949) found that with successive eggs in the four-egg set
the avocet incubated 75, 89, 97, and 100 per cent of the time. It is prob-
able that the incubating attentiveness is initiated by hormones, but it
may also require a contact stimulus from a full set of eggs and be cor-
related with the development of a brood patch. Full incubating attentive-
ness is normally developed by the time the set is completed and in some
species may occur well before the last egg is laid. The amount of incuba-
tion that the first eggs receive before the last eggs are laid affects their
intervals of hatching.
Once incubation is well established, it tends to remain more or less
uniform until the young hatch. In the studies here reported there is no
evidence that the incubating birds consistently spend more time on the
eggs during the latter days just before hatching. Air temperature affects
the attentive rhythm, however, and the coincidence of cold weather with
the latter days of incubation may explain observations reported in the
literature where the incubating birds appeared to sit more closely as in-
cubation progressed. |
An increase in tempo of the attentive rhythm commonly occurs with
the hatching of the eggs. Attentive periods tend to be shorter and to come
more frequently. As the young get older and mature physiologically,
brooding attentiveness progressively declines, but the rate of feeding
usually increases. With full active feeding of the young, attentiveness
170 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
may be just as intense as during the incubation phase of the reproduc-
tive cycle, even though definite periods of attentiveness and inattentive-
ness are more difficult to discern. However, after the young become
fledged, leave the nest, and become progressively more independent of
their parents, the attentive behavior of the adults gradually disappears,
and the birds have completed their reproductive cycle for the year.
Changes in air temperature cause important changes in the rhythm of
attentiveness from day to day. With a rise in air temperature, our data
show that there is almost always a decrease in the average length of the
attentive periods. There is simultaneously an increase in the total time of
inattentiveness, but this may be brought about either by lengthening the
inattentive periods or by increasing their number. Nice and Thomas
(1948) have summarized the literature for five passerine species and
make this same generalization in regard to the influence of temperature
on incubating attentiveness.
The effect of temperature on attentiveness is also evident in the daily
rhythm of attentiveness or the variations that occur from hour to hour.
In general, incubating and brooding attentiveness decreases until early
or mid-afternoon and rises again in the evening. The drop in attentive-
ness during the afternoon may be scarcely noticeable on cool days but
becomes pronounced on hot ones. The same rhythm of hourly variations
in attentiveness occurs in the feeding of the young, although it may be
less pronounced, and the late afternoon rise may not always appear.
Information is accumulating fairly rapidly on the daily rhythm of atten-
tive behavior in many species with the increasing tendency for bird
students to use automatic recording devices or to take all-day observa-
tions. Palmgren (1949) has recently made a useful summary of much
of this literature.
In those species where the female does all the brooding of the young
after hatching, the male may bring more food to the young than does
the female. As the young grow older and they need to be brooded less
frequently, the female is commonly the more attentive of the two sexes
to their feeding.
The rate at which the young are fed is affected by various factors,
especially by the age and number of young in the nest. There is general
agreement among most observers that the rate of feeding increases as
the young get older, but there is difference of opinion as to how much
the size of the brood affects the feeding rate and the length of the nest-
ling period.
Paynter (1949) found that herring gulls (Larus argentatus) feed broods
of three young just as easily and as efficiently as broods of one or two
because a surplus of food is always brought to the nest. Skutch (1949a )
transferred young between nests of the song tanager (Ramphocelus
ATTENTIVE BEHAVIOR OF MISCELLANEOUS SPECIES Al
passerii) and found that broods of one, two, and three were fed at rates
of 7, 15, and 21 times per hour or about seven times per young bird per
hour regardless of the number in the nest. However, this study was for a
very limited period. We found (p. 105) phoebes feeding a brood of
four young four times as rapidly as a brood of one young. Kluijver
(1950) found no relation between size of brood and rate of feeding in
the great tit, Parus major nor did Moreau (1947) find any differences
in the rate at which each young bird was fed in broods of different size
in the white-rumped swift (Apus (Micropus) caffer) and red-throated rock
martin (Ptyonogrogne fuligula). However, Moreau found from the study
of other species that “as a rule, the more young in the nest the more
frequent the parents’ visits, but not in proportion to the increase in the
number of young.” This conclusion is concurred in by Kluijver (1933),
Lack (1947-48, 51), Lack and Silva (1949), and Gibb (1950), and was
found with the house wren (p. 61) and robin (p. 130) in the present
study. Skutch (1949a) suggests that “the existence of an innate rhythm,
adjusted to the normal brood, would explain why each nestling in a
smaller brood is fed more often than each one in a family of the usual
size.” One adult house wren can easily care for small broods, but the
effectiveness of both adults participating increases greatly as the size of
the brood becomes larger.
There is evidence that the nestling period of the house wren is shorter
for small broods which are fed more frequently, than for large broods.
This relation has also been demonstrated for violet-eared hummingbirds
(Colibri thalassinus) by H. O. Wagner (1945) and for the paradise fly-
catcher (Tchitrea perspicillata) by Moreau (1947). Karplus (1949) found
that the nestling period of robins (Turdus migratorius) in Arctic Alaska
was reduced to 8.8 days compared with 18 days which is common for
temperate regions. He correlates the shorter nestling period of Arctic
birds to their being fed for 21 hours per day rather than 14 to 15 hours
per day farther south.
On the other hand, Paynter (1949) found no relation between nestling
period and size of brood in the herring gull, bu: this would hardly be
expected since he found no difference in the rate at which each young
was fed. In Moreau’s (1947) study of nine species, the paradise fly-
catcher, already referred to, was the only one that showed a relation
between the size of the brood and the length of the nestling period.
Although no substantiating data are presented, Moreau suggests that
although large broods may leave the nest after the same nestling period
as small broods, they may weigh less at this time. Lack and Silva (1949)
found in the European robin (Erithacus rubecula) that undernourish-
ment caused a decrease in the weight of the birds at the time of leav-
ing the nest and that the nestling period was not prolonged. Lees ( 1949)
172 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
records that in this species broods of four or five sometimes average
greater in weight than broods of either two and three or six and seven.
Gibb (1950) found in Parus major and P. caeruleus, however, that indi-
viduals in large broods averaged less in weight than individuals in small
broods. It would seem, therefore, that individual nestlings in large broods
may often receive less food than individual nestlings in small broods. As
a consequence their growth in weight is retarded. This may result in
either a prolonged period in the nest or in a lower weight, if the nest is
vacated at the normal time. There are characteristic differences between
species in the manner in which these variations occur.
Koskimies’ (1950) studies on the swift, Apus (Micropus) apus, are of
interest in this connection. The nestling period in this species varies
between extremes of 33 and 56 days dependent on the weather, although
it is more usually 40 to 43 days. This great variability is due to the rate of
feeding the young and consequently the time required for them to attain
normal final weight being directly correlated with air temperature.
V. Evolution of Parental Care
INTRODUCTION
The foregoing analyses of details in the parental care of several species
of birds demonstrate that important variations in behavior pattern exist.
One immediately wonders how these variations in behavior came about
and their relation to each other. Perhaps they show a phylogeny in the
same manner as do structural characteristics of the body. Possibly, differ-
ent behavior patterns of parental care develop in different environmental
situations.
Curiosity in regard to these possibilities led to a summarization of the
literature on the known parental behavior for the bird families of the
world. This has been no small undertaking, but I have had the help of
various assistants, particularly Dr. Frank A. Pitelka, Dr. J. Murray Speirs,
and Dr. Ben J. Fawver. Attempt was made to cover completely the litera-
ture on North American birds. A systematic search was made through all
important journals and other available literature as far back at least as
1930 for the rest of the world. For still earlier data on foreign birds, re-
liance has been placed on the summaries of Witherby et al. (1938-1941),
Niethammer (1937-1942), Groebbels (1932-1937), Stresemann (1927-
1934), and Knowlton (1909). For North America the summaries of
Burns (1915) and especially Bent (1919-1950) have been most helpful.
The present summary should bring information on parental care up to
date to the year 1950. At this point, we wish to make special acknowledg-
ment of the splendid studies of Alexander F. Skutch on Central American
birds, of R. E. Moreau on African birds, and of L. E. Richdale on
marine birds, which in many instances have been the only sources of
information for some of the less widely distributed families. I wish also
to acknowledge the special help given by Mrs. Margaret M. Nice in
correcting incubation periods given in Table 51 as a result of her thorough
review of the literature on this problem.
The most critical information in establishing the parental behavior
pattern for a species or for a family has been the share of the sexes in
nest building and incubation, the length of attentive periods on the
eggs, and the care of the young. For many families the information is
very general. For families of higher phylogenetic rank the information is
both more complete and more detailed. Data on length of time required
for nest building, number of eggs laid, length of the incubation period,
and the length of the nestling period are compiled mainly for those spe-
a A>)
(9
174 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
cies where information is available on parental care, and usually, then,
only when given by the author in his particular study. This should render
correlations between these two sets of factors more trustworthy than if
the compilation were of a more general sort. Furthermore, to render such
a general compilation of greatest value one would need to distinguish dif-
ferences due to race, latitude, climate, seasonal and yearly variations, and
other factors which are extraneous to the present objectives. Incidentally,
topics not touched on at all in the present work are the roles of the two
sexes in the selection of nest sites (Nethersole-Thompson, 1943) and in
nest sanitation (Blair and Tucker 1941, Tucker 1941).
The term “nestling period” rather than fledgling period will be used to
designate the time that the young bird remains in the nest (Moreau
1946). There seems to be considerable confusion as to the use of “fledg-
ling period,” since “almost as much development toward complete fledg-
ing takes place after the nest is quitted as during the stay in it” (Ryves
1944). Fledging commonly means to become fully feathered and able to
fly, but this more often than not fails to coincide with the time the young
bird leaves the nest.
We have used Peters’ Check-List of Birds of the World (1931-1948)
for arranging and classifying the data on nonpasserine species, and we
have similarly used Wetmore’s A Revised Classification for the Birds
of the World (1951) for the Passeriformes. Nomenclature follows Peters
for the orders below the Passeriformes, and Witherby et al. (1938-41)
and the A. O. U. Check-List of North American Birds (1931), along with
its later supplements in The Auk, for the Passeriformes. When the name
given by the author of a paper does not agree with these authorities, it
is shown in parentheses, so that there should be no confusion concerning
the species concerned. Observations are included on all living orders of
birds except the Coliiformes, although the information available on
some groups is scant.
Comparative psychologists commonly organize their information in an
evolutionary sequence (Washburn 1923; Warden, Jenkins, and Warner
1934). Likewise, there have been attempts to outline the stages in the
evolution of certain types of behavior (e.g., Allee 1938 ). Nevertheless, the
actual tracing and analysis of behavior patterns as they develop from one
group of animals into another have not been frequent. This has been done
for social insects by Wheeler (1928), and Emerson (1938) has been
able to do this for termites, using the nest structures in these latter insects
as the morphological expression of behavior patterns. Emerson found
the nest-forming behavior to be predominantly an inherited species
pattern, and sequences of species patterns indicated evolutionary progress
within the genus or related genera that could be correlated with the
known morphological evolutionary relationships of the species. Astonish-
EVOLUTION OF PARENTAL CARE 175
ing examples occurred of adaptive modification of the nests together with
convergent evolution of nest structure in certain environments which
gave evidence of the force of selection upon inherited patterns. K. Lorenz
(1941) and Delacour and Mayr (1945) have used behavior patterns as
evidence for showing the proper relations and classification of the
Anatidae.
The objectives of this study are to trace the evolution of the behavior
pattern concerned with parental care through the class, Aves; to attempt
to find underlying trends that will enable us better to correlate the be-
havior of related species; and to interpret the forces and influences that
were and are effective in bringing about the patterns as we now see them
in the various groups.
SUPERORDER: PALAECGNATHAE; ORDER: STRUTHIONIFORMES
Family: stRUTHIONIDAE. Watson (1905) has described the nesting be-
havior of captive ostriches, Struthio camelus, in Arizona. The nest is a
round hole in the ground which the male scoops out with his feet. At
first the female may not take to the nest but may lay her eggs on the
ground, whereupon the male will roll them into the nest. Generally, after
the male has put three or four eggs into the nest, the female will lay
there. In about thirty days she will lay twelve to sixteen eggs and will
commence incubation. The incubation period is about 42 days. The male
takes a prominent part, covering the eggs 15 or 16 hours a day. He usu-
ally goes on the nest about 1700 and remains until 0800 or 0830 hours
the next morning; the female takes her turn during the day. According to
Schneider (1949), the male does all the incubation. The male usually
begins sitting three or four days before the female stops laying. If the
weather is cold during the laying period, the male may often be found
covering the eggs at intervals during the night. The birds are also very
watchful in the warm season to prevent the eggs from becoming over-
heated by the sun. Often one of the adults will be found sitting on its
ankle joints with both wings extended to shade the eggs. At the time
of hatching, the parent bird is described as cracking the shell with its
breastbone and sometimes taking the young bird by the head and pull-
ing it out. Sometimes three or four days elapse between the hatching of
the first and last eggs in the set. During this time one of the parents
takes care of the precocial chicks while the other is attentive to the nest.
ORDER: RHEIFORMES
Family: RHEDAE. Headley (1895) states that the female rhea, Rhea
americana, lays a great number of eggs and that several females may lay
in one nest. Adams (1908) noted that a captive female laid every three
days. When a certain number of eggs have accumulated, one of the males
176 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
takes over, and the female starts another nest. Incubation requires five
or six weeks. The male not only does all the incubating but also takes care
of the precocial young. Portielje’s (1925) observations on captive birds
showed that the male began incubation at one nest after the female had
laid her fourth egg. The male occasionally left the nest to drink and feed
during the middle of the day, and while the male was away the female
was seen visiting the nest.
ORDER: CASUARIIFORMES
There are two families of living birds in this order. Detailed informa-
tion on the nesting behavior of Casuariidae is not available, but sup-
-posedly only the male incubates.
Family: pRoMIcEmMDAE. The behavior of captive emus, Dromiceius n.
hollandiae, has been studied by Crandall (1929) and Fleay (1936), and
birds under natural conditions have been studied by Gaukrodger (1925).
Sometimes two or three females will lay in the same nest, and there may
be seven or eight eggs. The male incubates, beginning with the last egg,
and he rarely leaves the nest. The incubation period is 58 to 61 days.
The male also cares for the young.
ORDER: APTERYGIFORMES
Family: ApTERycIDAE. The most complete information on the kiwi,
Apteryx sp., was obtained by Robson (1948) from a pair of birds which
he held captive several years. This species under natural conditions ex-
cavates a burrow for nesting. Robson states that both sexes dig, not just
the female as is frequently stated in the earlier literature. The male bird,
however, does almost all of the nest building.
The female laid two to five eggs in different years, but apparently not
more than three were incubated at one time. The regular incubation
period was found to be 75 days, although 77 days may be required for
the first egg in a two-egg set. In one instance, the female sat on a freshly
laid egg for 3 days, going out for food only at night. The male took ex-
clusive charge of incubation thereafter. The second egg was not laid
until 11 days after the first. The male incubates steadily, and may not go
off the nest for a week at a time. When he is inattentive he covers the
eggs, and when he returns he brings additional nesting material.
The chick is precocial at hatching, but its feathers do not become free
of a slimy material for 4 or 5 days, and it does not leave the nest until
the sixth day. During these 6 days the male blocks off the opening to the
nest cavity and takes exclusive charge of the young. The chick loses
weight while confined to the nest, but when it becomes free it eats an
enormous amount, both day and night. The old birds feed only at night.
EVOLUTION OF PARENTAL CARE Leey.
ORDER: TINAMIFORMES
Family: TrInamipaE. According to Seth-Smith (1907) and Daglish
(1930), the male tinamou takes charge of the eggs as soon as they are
laid and incubates them. His mate goes off to court another male, only
to leave him in due course with another potential family. The female
tinamou is more brightly colored than the male, and the usual sexual
courtship role is reversed. Beebe (1925) found an average sex ratio of
four males to one female in Crypturellus (Crypturus) variegatus. No nest
is made except for a slight depression on the forest floor. In this species
the female, after courting the male, lays a single egg and then leaves the
male to do all the incubating. The incubation period is about 21 days, and
the young bird leaves within a day after hatching. The male takes care
of the chick. Very soon, however, he may start incubating another egg,
and this cycle may continue even for a third egg. Seth-Smith (1907)
found C. tataupa and Calopezus elegans also polyandrous under aviary
conditions. The behavior pattern in Tinamus is different in that the male
incubates only one set, but this may contain from four to twelve eggs.
SUPERORDER: NEOGNATHAE; ORDER: SPHENISCIFORMES
Family: sPHENIScIDAE. Richdale has made detailed studies of the pen-
guins, Eudyptula minor (1940), Megadyptes antipodes (1941b, 1949b,
1951), and Eudyptes sclateri (1941a); Bagshawe (1938) and B. Roberts
(1940b) have studied Pygoscelis papua and Levick (1914), P. adeliae.
Murphy (1936) has summarized information on several species. The
group as a whole is very colonial in its nesting behavior, although in
some species (M. antipodes, two species of Eudyptula, and perhaps
others ) the nests are somewhat scattered. Both sexes aid in nest building,
and the nest may be composed of debris or stones or it may be a burrow
in the ground. Usually two eggs are laid within 2 to 5 days. Incubation is
shared by both sexes and may begin with either the first or second egg.
The incubation period varies from 5% to possibly 8 weeks in different
species. Attentive periods between 6 and 12 hours are reported in
Spheniscus magellanicus, S. demersus, and Eudyptes sclateri, but be-
tween | and 5 or more days in Eudyptes crestatus, Eudyptula minor,
Megadyptes antipodes, Pygoscelis papua, and P. adeliae. Bagshawe
(1938) found the male P. papua on the nest for periods of 1 to 2 hours
and the female for 3 to 14 hours before the first egg was laid, both sexes
on for periods of 5 to 15 hours between the laying of the first and second
eggs, and for periods of 6 to 31 hours after the second egg was laid. In
P. adeliae, Levick (1914) reported the female on the egg for 13 days
followed by the male for 14 days, but the accuracy of his recognition of
the sexes has been questioned.
178 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
After hatching, the young are brooded for 2 to 4 weeks and are fed
once or twice a day. The nestling period varies from 8 to 16 weeks. The
young are constantly guarded during the daytime for only part of this
period—6 to 7 weeks in M. antipodes, 4 to 6 weeks in E. minor.
In several species, such as Aptenodytes patagonica, Pygoscelis adeliae,
P. papua, and Eudyptes crestatus, a communistic arrangement appears |
to develop for the care of the young as they get older. From 12 to 20
young birds are grouped together into “creches” and are guarded and
shepherded by a few adult birds. This permits both parents of many
of the pairs to hunt food at sea at the same time. When the parents
return, it is uncertain whether they recognize and feed only their own
young, but they may come back each time to the same area. In Apteno-
dytes forsteri, the communistic system is different in that there appears
to be a surplus number of broody adults in the colony. No sooner does
a parent leave its egg or young than a scrimmage takes place between
many free adults to determine which will have its turn at caring for it.
Thus old birds, other than the two parents, take turns at attending the
egg and chick. Richdale (1951) questions the whole concept of creches:
He believes that the parents feed only their own young and that the
extra adult birds present are nonbreeding individuals.
ORDER: GAVIIFORMES
Family: GAvupar. Surprisingly little attention has been paid to the
nesting behavior of loons or divers. A nest is built and two eggs are laid
with an interval of at least two days between them; incubation begins
with the first egg and lasts 28 to 30 days. Both sexes usually alternate
at incubating and taking care of the precocial young (Bent 1919, With-
erby et al. 1940), but in Gavia (Colymbus) stellata, Van Oordt and Hux-
ley (1922) and Keith (1937) found only the female on the nest.
ORDER: COLYMBIFORMES
Family: co.ympmwar. Huxley (1914) found in the grebe, Colymbus
(Podiceps) cristatus, that the nest is built in a few hours. Both sexes took
part, averaging between them more than two loads of weeds to the nest
every minute, maintaining this rate for a half hour or an hour at a
stretch. Three to seven eggs make up a set in various species. Some-
times two days elapse between consecutive eggs, and incubation com-
monly begins with the first egg (Niethammer 1938). Both sexes alternate
at incubating. Deusing (1939) found in Podilymbus podiceps that the
male’s attentive periods on the eggs averaged 29 minutes and the female's
40 minutes. The eggs were left unattended an average of only 8 minutes
at a time, and were usually covered with vegetation. The female con-
tinued to add nesting material through the incubation period. Witherby
EVOLUTION OF PARENTAL CARE 179
et al. (1940) record that in Colymbus auritus the sexes were observed
changing on the eggs at intervals of four to five hours. In Colymbus
(Podiceps) nigricollis the interval is one to three hours (Groebbels 1937 ),
in Colymbus (Podiceps) ruficollis about 40 minutes (Hartley 1933) or
20 to 30 minutes (Mountfort 1934). The incubation period in several
species appears not to have been accurately determined for natural con-
ditions, but it is believed to be 21 to 23 days; Harrisson and Hollom (1932)
give it as 27 to 29 days in C. cristatus; Mountfort (1934) found it
very variable, 18 to 26 days in C. ruficollis. The young grebes leave the
nest very soon after hatching and are attended by both parents. Probably
the female is somewhat more solicitous in their care, especially as they
grow older. Bird (1933a) observed that young Colymbus ruficollis would
return to the nest until almost fully fledged. E. Ashby (1933) and Little-
johns (1936) give additional observations on this species.
ORDER: PROCELLARIFORMES
Family: DIOMEDEIDAE. Richdale’s (1939, 1942a,b) observations on the
royal albatross, Diomedea epomophora, indicate a very slow rhythm of
nesting behavior. The birds breed only every other year unless there has
been a nesting failure. Both sexes aid in the building of a simple grass
nest. One egg is laid. Both sexes incubate with very long attentive periods
varying from 1 day to as long as 14 days. The average length of 43 atten-
tive periods that were measured (30 given by Richdale 1942b: 253; 13
more obtained through correspondence with him) is 5.3 days. The incu-
bation period is 78-80 days. The chick may require 3 days to get out of
the shell. The young bird is fed daily by regurgitation in its very early
days, even though the parent may not have left the nest for several days.
The usual rate of feeding for the first three months is twice per week,
once by each parent. The chick is guarded and brooded for 33 to 42
days after hatching by one or the other parent in attentive periods that
average 3.4 days, a little shorter than during incubation. When the
feathers begin to crow, the young bird is fed five times a week and may
be left alone for long periods of time. Considerable food is given at a
time, often 1.5 pounds; occasionally up to 6.5 pounds when both parents
feed it. Feedings take place during the daytime. The chick stays aground
until its wings have reached an adequate length, which may be 229 to
251 days after hatching. When fledged, during the last two weeks the
feeding rate is again reduced to twice per week. Probably the nesting
behavior of other albatrosses is similar. In D. bulleri, Richdale (1949a)
records that nest building may be performed by either sex but usually
by the male. The first attentive period of the female after the egg is laid
averages 5.9 days, but subsequent periods by both sexes are equal and
average 10.8 days. The longest observed period of a female was 24 days.
180 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Richdale (letter) cites a still more remarkable record for the Laysan
albatross (D. immutabilis) where the average attentive period subse-
quent to the first span by the female from 64 records is 21.8 days, range
5 to 32 days!
Family: PROCELLARUDAE. In the subfamily, Fulmarinae, Richter (1937)
found the incubation period of the fulmar, Fulmarus glacialis, to be 57
days. Each parent sits on the one egg in its shallow nest for attentive
periods that average 1 to 2 days in some cases or 4 days in others. The
young are brooded continuously for two weeks but are largely left
alone in the nest after 5 weeks. The nestling period is 57 days, and the
young is fed once each day until nearly ready to fly. In a personal com-
munication, Richdale states that the young is fed during the daytime.
Richdale (1944b,c) found the incubation period of the one egg in
the nest burrow of Pachyptila turtur and P. forsteri (vittata) to be 56
days and the nestling period about 49 days. The attentive periods for
the two parents alternating on the nest are 6 or 7 days long. During the
first 3 to 5 days after hatching, the young are sometimes fed during the
daytime, but after that, only at night. Occasionally both parents feed
the chick on the same night, but some nights are skipped by both adults.
Considerable food is regurgitated each time, and the chick may some-
times receive an amount equal to its own weight.
In the subfamily, Puffininae, Lockley (1942) has studied the Manx
shearwater, Puffinus puffinus, Richdale (1944a, 1945b) the sooty shear-
water, P. griseus, and Glauert (1946), the little shearwater, P. assimilis.
These birds nest in underground burrows which both sexes excavate.
One egg is laid, and the incubation period is 51 to 58 days. The male and
female take turns incubating at intervals of about 2 days in P. assimilis
and 4 days in the other two species, although an occasional attentive
period in P. griseus may be as long as 13 days. Brooding is required
for only a very few days. For the first 3 to 7 days after hatching, the young
chick may be fed during the daytime, but after that, only at night as
these birds, like Pachyptila, are largely nocturnal in this habit. In P. assim-
ilis the young bird is fed usually every second night. The adult birds
spend the daylight hours in activities far out at sea. Sometimes both pa-
rents may feed the young on the same night; then again the bird may not
be fed for periods up to 10 nights. Individual feedings are considerable
and the young chick may sometimes consume its own weight of food.
The young bird is usually not fed for 7 to 13 nights before it finally takes
flight, 70 to 95 days after hatching.
Family: HyDROBATIDAE. Of the storm petrels, Oceanites oceanicus has
been studied by B. Roberts (1940a), Hydrobates pelagicus by Lockley
(1932), Pelagodroma marina by Richdale (1943-44), and Oceanodroma
leucorhoa by Gross (1935) and Ainslee and Atkinson (1937). Both
EVOLUTION OF PARENTAL CARE 181
sexes participate in excavating the nesting burrow, although in Leach’s
petrel, O. leucorhoa, the male takes the major part and about 3 days are
required. Only one egg is laid and incubation may begin immediately or
after a lapse of 24 hours. Both male and female incubate in relays of
1 to 5 days. Nest relief occurs at night. There may be periods as long as
4 days when neither bird is on the egg; on the other hand, one parent may
occasionally be attentive for as long as 9 continuous days. The incubation
period is between 38 and 50 days long. After the young bird hatches, it
is brooded for only 1 to 5 days. The down on these chicks is long. While
brooding, the chick may be fed during the day as well as at night, but
thereafter the parents usually visit and feed it only at night. Feeding is
somewhat irregular, as frequently the young bird may not be fed for
several nights in succession, especially near the end of nest life. In O.
leucorhoa the average rate is once per night. The nestling period lasts
about 8 weeks.
Family: PELECANOIpIDAE. In the diving petrel, Pelecanoides urinatrix,
Richdale (1943, 1945a) found both sexes digging the burrow. He esti-
mates the incubation period to be 8 weeks with the male and female re-
lieving each other nightly. After hatching, the young bird is fed nightly
and often also in the daytime during the 7- to 15-day brooding period.
This longer brooding period may be correlated with shorter down than
in the storm petrels. After brooding is over, one or both parents feed the
chick only at night, until it is ready to leave the burrow after about 54
days from hatching.
Summary. Both sexes construct the nest, incubate, brood, and feed the
young. Only one egg is laid, and the incubation period is from 7! to 9
weeks except in Diomedeidae where it is over 11 weeks. The young bird
is brooded for only a few days except in Diomedeidae, but it stays in the
nest 7 to 12 weeks, except in Diomedeidae where it may not leave until
eight months old. Average attentive periods during incubation com-
monly vary from | to 7 days in length. After the young bird hatches it is
usually fed by both parents at night except in Diomedeidae and Ful-
marinae and possibly some petrels, but there is considerable irregularity.
These species are largely nocturnal in their nesting activities and spend
the daylight hours out at sea. The slower rhythm of the larger Diome-
deidae is evident as the young is fed only two to five times per week.
This group is also more diurnal in its activities, so in several ways its
behavior does not conform exactly to the procellariiform pattern.
ORDER: PELECANIFORMES
Suborder: PHAETHONTES; Family: PHAETHONTIDAE. In the yellow-
billed tropic-bird, Phaéthon lepturus, a single egg is laid and both sexes
alternate in its incubation (A. O. Gross 1912). Au adult was once ob-
182 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
served feeding its incubating mate, and apparently this interfeeding of
the adults also occurs in P. aethereus (Bent 1922). Twenty-eight days are
required for incubation, and the young bird remains in the nest for 62
days. The adult birds spend considerable time with the young for the
first 10 days, but after 20 to 25 days they feed the young two or three
times in the early morning and do not appear again until the next day.
Suborder: PELECANI; Superfamily: PELECANOIDAE; Family: PELECANIDAE.
The pelicans lay two or three eggs. Incubation has been estimated at
4 to 6 weeks. Both sexes share the incubating duties, and there is a cere-
mony of nest relief (Bent 1922). The young stay in the nest for 2 to 5
weeks. According to Murphy (1936), the young of Pelecanus occidentalis
may be fed at any hour but particularly between 0700 and 0800 hours,
shortly before noon, and during the two hours before sunset. The young
of P. conspicillatus become gregarious as soon as they leave the nest,
occurring in flocks of 10 to 50 birds ( Macgillivray 1923).
Superfamily: suLowEA; Family: sutmar. In the boobies, Sula, and in
the gannet, Morus bassana, only one egg is laid, or a second may be
deposited after an interval of several days. Both sexes share nest build-
ing, incubation, brooding, and feeding the young. Griffin and Hock
(1949) record that the attentive period on the eggs in Morus is 24 hours,
with variation between 7.5 and 30 hours. One bird, whose mate was re-
moved, stayed on the eggs for 3 days. As nests of Sula are often fully
exposed to the sun, incubating and brooding may be more a matter of
keeping the eggs and young cool through shading than of keeping them
warm (Murphy 1936). At night, the mate of the brooding Sula stands
alongside the nest. After the young bird becomes too large to brood, it
may pass the night on the ground between the two parents (Chapman
1908). The length of incubation is probably 42 to 45 days. The period
that the young are fed by their parents is as long or longer. The young of
Morus are fed more frequently in late afternoon, and,not often during
the middle of the day (Wodzicki and McMeekan 1947). Some 10 or more
days before the young leave, the parents stop feeding them, and appar-
ently the lack of food is a stimulus for the birds to begin shifting for
themselves.
Family: PHALACROCORACIDAE. In the double-crested cormorant, Phal-
acrocorax auritus (H. F. Lewis 1929, Mendall 1936), the males bring
nest material, and the females shape it into a nest in from 2 to 4 days.
Usually one egg is laid each day, until the set of about four is complete.
Incubation may begin with the first egg or irregularly with any subse-
quent egg. The incubation period is 24 to 25 days, the young are brooded
until the third week after hatching, and fed until they are 5 or 6 weeks
old. Both sexes incubate, alternating on the nest during the day at one-
to three-hour intervals. Both sexes brood and feed the young. Two or
EVOLUTION OF PARENTAL CARE 183
three young are fed on each trip with trips about once every hour.
Family: ANHiNcIDAE. Not much is known about the nesting of Anhinga
anhinga. The four eggs are laid at irregular intervals and both sexes take
part in their incubation. Both male and female care for the young.
Suborder: FREGATAE; Family: FREGATIDAE. Both sexes of Fregata mag-
nificens, the man-o’war-bird, share in nest building, incubating the one
egg, brooding, and feeding the young. There is no information, however,
on the length of the attentive periods (Murphy 1936).
Summary. The nesting cycle of these colonial birds is long, since it
frequently extends over three months. There is considerable uniformity in
behavior in that both sexes share more or less equally in all the duties of
nesting. In the Phalacrocorax the attentive period is only 1 to 3 hours long
while -incubating, but in Morus it may be 24 hours long. One to four
eggs are laid, separated often by intervals of several days. It is usual for
most of the brood to be fed on each trip. These trips may be as frequent
as once per hour in Phalacrocorax, but as the young get older they tend
to be limited more and more to early morning and late afternoon.
ORDER: CICONIIFORMES
This is a varied order that has been divided into four suborders. The
Ciconiae is the largest and is again subdivided into three superfamilies
each with a single family. No data are available for the suborder Balaeni-
cipites, with its single family, nor for the family Cochleariidae of the
Ardeae.
Suborder: ARDEAE; Family: arpempaAE. The herons or Ardeinae com-
monly nest in colonies. Both sexes take part in nest building. Three to
five eggs are laid, usually at 2- or 3-day intervals. Incubation begins with
the first egg. Estimates as to the length of incubation vary from 18 to 28
days, but the exact time is not known for many species. Both sexes alter-
nate at incubating at intervals of two to six hours during the day, and
an elaborate ceremony has developed when one sex relieves the other.
Probably the female is on the eggs at night. Brooding may last 2 or 3
weeks, and the young may remain a few weeks longer before leaving.
Both sexes bring food to the young at the rate of 6 to 14 times per day.
Feeding is most active in early morning and evening. Nycticorax, Nyctan-
assa, and Ardea herodias are more or less active at night as well as dur-
ing the day (Bent 1926, Witherby et al. 1939, Gersbacher 1939, Steinfatt
1934b, 1935, 1939e, Allen and Mangels 1940). The rhythm in the African
green heron, Butorides striatus (atricapilla), is faster than above out-
lined. Cowles (1930b) states that the incubation period is about 18
days, the nestling period is only 2 weeks, and the young are fed three
times per hour at first but that later this rate slows down. Hindwood
(1933), however, found the incubation period of Butorides javanica to
184 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
be 21 days and the nestling period about 4 weeks. Wheelock (1906)
observed a feeding rate in Butorides virescens of about three times per
hour for young 7 days old but only for the early morning and evening
hours.
The behavior of bitterns, Botaurinae, is similar to that of herons. The
four or six eggs are incubated by both sexes in Ixobrychus but apparently
only by the female in Botaurus (Bent 1926, Groebbels 1937). Groebbels
(1935) recorded four attentive periods for the female Ixobrychus minutus
averaging 2 hours 23 minutes and five periods for the male averaging 1
hour 6 minutes. Incubation in this species lasts 16 to 17 days, and in
Botaurus stellaris, 25 to 26 days. Young Ixobrychus may leave the nest
in 7 to 12 days (Niethammer 1938). Young Botaurus lentiginosus stay
in the nest for 14 days (Mousley 1939). Gabrielson (1914) found two
young fed at the rate of 0.6 times per hour, but both young are fed on
each visit of the adult. Niethammer (1938) records the nestling period
of B. stellaris as 4 to 5 weeks, which seems very long.
Suborder: C1CONIAE; Superfamily: scopowaE; Family: scopwar. Cow-
les (1930a) describes the nest and development of young of the hammer-
head, Scopus umbretta, but does not tell much concerning their attentive
behavior. It appears that both sexes are involved in various phases of
nest life. The incubation period is about 21 days, and the young stay in
the nest about 7 weeks.
Superfamily: crcontoweEA; Family: crconupar. According to Nietham-
mer (1938) and Witherby et al. (1939), the nests of both storks, Ciconia
ciconia and C. nigra, are build by both sexes, the male bringing most of
the material and the female arranging it. The building of a complete nest
may require 8 days. The three to five eggs are laid at 2-day intervals.
Incubation begins with the first or second egg and lasts 30 to 38 days.
In the former species the female incubates all night, while during the day,
the male assumes the greater part of this duty. The two sexes alternate at
one to four and a half hours (Nice 1933, Schiiz and Schiiz 1932, Schiiz
1938). The nestling period is about 63 days. Both sexes brood and care
for the young. In C. nigra the parents relieve each other at intervals of
two and a half hours when the young are 3 weeks old. Five meals are
brought to the young daily, two in the early morning and three late in
the day. In C. ciconia, Schiiz (1943b) found the feeding rate of young
5 to 15 days old to average 0.7 per hour but often with long intervals be-
tween consecutive feedings. Both sexes also incubate in Jabiru mycteria
(Bent 1926).
Superfamily: THRESKIORNITHOIDEA; Family: THRESKIORNITHIDAE. Bay-
nard’s (1913) detailed study of the glossy ibis, Plegadis falcinellus, shows
that both sexes aid in the construction of the nest which is added to
‘EVOLUTION OF PARENTAL CARE 185
throughout the incubation period. An egg is laid each day until three or
four eggs are laid. Incubation does not start until a day after the last
egg has been laid and lasts 21 days. The female sits on the eggs at night
and until 0830 or 0900 hours in the morning. The male relieves the female
for about six hours during the day. During the first 4 weeks after hatch-
ing, the adults feed the young 12 to 20 times per day. By the sixth week
the young are leaving the nest during the daytime and feeding in the
shallow water but returning to the nest to roost at night. The glossy ibis
belongs to the subfamily Threskiornithinae.
The behavior of the roseate spoonbill, Ajaia ajaja, of the subfamily,
Platoleinae, is very similar (R. P. Allen 1942). The average clutch is less
than three eggs, probably one laid every other day, and the incubation
period is 23 to 24 days. There is a ceremony at nest relief which occurs
at least two or three times during the day. Incubation is not regular until
the last egg is laid. |
Suborder: PHOENICOPTERI, Family: PHOENICOPTERIDAE. Only one egg
ordinarily is laid by flamingos, Phoenicopterus ruber. Chapman (1905)
says that the two sexes exchange places on the eggs in the early morning
and late in the afternoon. There is considerable irregularity as to which
sex is on the nest during the daytime and at night. Bent (1926) indi-
cates that the incubation period is 30 to 32 days. The young are brooded
for 3 or 4 days and then they leave the nest. They are fed by the adults
for about 2 weeks (Gallet 1948 ).
Summary. There appears to be considerable uniformity in attentive
behavior in this order of colonial nesting birds. Both sexes share all
phases of nesting duties. During incubation and brooding the sexes re-
lieve each other with elaborate ceremonies at intervals of one to several
hours. Feeding of the young is largely by regurgitation and all the
young may be fed on each visit. The length of the incubation period
varies greatly between species as does the nestling period.
ORDER: ANSERIFORMES
Quite a little general information is available for this order. In the
family, Anatidae, of the Anseres, only the subfamilies, Plectropterinae,
Cereopsinae, and Merganettinae cannot be included in the discussion,
but they are small groups.
Suborder: ANHIMAE; Family: ANHIMIDAE. Stonor’s (1939) observations
on the nesting of the screamer, Chauna torquata, in a zoological garden
are of interest here. Both sexes participated in nest construction and in
incubation. Eggs were laid on alternate days, and there were as many as
six eggs in a set. The female incubated from late afternoon, 1630 or 1730
hours, overnight or until 0900 or 1100 hours the next day, when the male
186 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
took over for the rest of the day. There was a ceremony of nest relief. The
incubation period was 6 weeks, and the young left the nest soon after
hatching.
Suborder: ANSERES; Family: ANATIDAE. Swans, in the subfamily Cygni-
nae, lay four to six eggs on alternate days in a nest which both sexes
have been concerned in preparing. Incubation may not begin until the
set is complete; it lasts 35 days or longer and is performed chiefly by the
female. Ruthke (1941) observed incubation to begin with the fifth of a
seven-egg set in Cygnus olor. Groebbels (1937) records both sexes incu-
bating in Chenopis (Cygnus) atrata and Cygnus melanocoriphus. Both
sexes care for the young, and the family group may retain its identity
for several months (Bent 1925, Witherby et al. 1939).
With the geese, Anserinae, the set in Branta canadensis is commonly
composed of four to six eggs, laid on consecutive days or at average inter-
vals of 1.5 days. Incubation begins when the set is complete and lasts
from 24 to 28 days in various species. The female makes the nest, but
the male sometimes will bring material for it. Only the female incubates,
although Soper (1942) believes that the male may take part in Chen
caerulescens. In nearly all species the male remains close to the nest and
is attendant on the female during incubation. Both adults care for the
young. During the nonbreeding season, geese commonly feed during
early morning and late afternoon and roost at night (Bent 1925, Kort-
right 1942, Kossack 1950, Manning 1942, Sutton 1932, Witherby e¢ al.
1939).
Little is known concerning the nesting behavior of the tree ducks,
Dendrocygninae. According to Bent (1925), Dendrocygna autumnalis
commonly nests in tree hollows, but D. bicolor mostly nests on the ground.
The former species has 12 to 16 eggs per set, but the number in the
latter species may reach 36. There is some possibility that several females
may lay in the same nest. Delacour and Mayr (1945) state that the male
shares in incubation; in fact, in D. viduata and D. bicolor he may do the
greater share. J. C. Phillips (1922) gives the incubation of the former
species as 28 to 30 days. Both sexes take care of the young.
In the surface-feeding ducks, Anatinae (Bent 1923, Kortright 1942,
Girard 1939, 1941, Bennett 1938, Munro 1944, Witherby et al. 1939),
the female prepares the nest, commonly lays 7 to 12 eggs for a set, de-
positing one each day, and begins steady incubation when the set is
completed. The incubation period varies between 21 and 28 days. The
female does all the incubation, although rarely a male has been known
to take a turn. Usually the male deserts the female after incubation gets
well underway so that the female must care for the young alone. In
Anas (Querquedula) cyanoptera, Anas crecca, Aix, Spatula, Tadorna, and
Casarca, however, the male is more faithful and may aid the female in
EVOLUTION OF PARENTAL CARE 187
caring for the young. The same has been observed for Anas platyrhynchos
(Lloyd 1937). Bennett (1938) says that the female blue-winged teal,
Anas (Querquedula) discors, during incubation is inattentive once or
twice a day for 20 minutes to two hours around 0700 and 1900 hours.
Each time she leaves she covers the eggs with nest down, and during
the last 48 hours of incubation may not leave at all. Girard (1941) found
that the female mallard, Anas platyrhynchos, had a feeding period of
about two hours between 0630 and 0830 hours and again in the after-
noon or evening. During the migratory and wintering seasons, these
ducks along the Illinois River in Ilinois roost on the water during the
day and feed during the night. D’Ombrian (1944) had black ducks
(Anas superciliosa) nesting under captive conditions. The female made
the nest and took full care of the eggs and young. She left the eggs for
average inattentive periods of 20.6 minutes, 0.9 times per day. There were
no regular times when she was inattentive, but they were equally divided
between morning and afternoon. Four months after the young hatched,
the female lost interest in them. Frank Bellrose (personal communica-
tion) has observed two inattentive periods, in early morning and late
afternoon, in the wood duck, Aix sponsa. Heteronetta atricapilla is unique
in that it does not build a nest and has become entirely parasitic, laying
its eggs in the nests of a variety of other species (Phillips 1925).
The behavior of the diving ducks, Nyrocinae, is similar to Anatinae
(Bent 1925, Kortright 1942, Witherby et al. 1939). Sets of eggs are often
smaller, sometimes only five or six eggs. The incubation period is com-
monly 25 to 28 days. The male usually deserts the female soon after the
eggs are laid, or at least by the time the young hatch. Murphy (1936)
states, however, that in Tachyeres branchyptera both sexes lead the
brood to sea, forming a family group which does not break up until
autumn. In the eider, Somateria mollissima, the female may be inatten-
tive for about two hours soon after daybreak (A. O. Gross 193°%a), but
some individuals apparently stay on their eggs continuously (Goodwin
1948). Gudmundsson (1932) maintains that during her early morning
inattentiveness the female drinks and bathes but does not eat throughout
the period of incubation. Bucephala (Glaucionetta) islandica females are
to be observed feeding between .0900 and 1100 hours. Low (1945) used
an itograph arrangement on the redhead, Nyroca americana, and found
that the eggs were unattended during the laying period and that incuba-
tion usually began within 24 to 48 hours after the last egg was laid.
Inattentive periods of the incubating female came at irregular intervals
during the day and night. The birds left the nest from 3 to 26 times,
averaging 6 times, during the 24-hour period. Prevailing temperatures
affected the time on and off the nest; as much as seven hours per day were
spent off the nest for first nests and nine hours for later nests. Hochbaum
188 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
(1944) also found in the canvas-back, Nyroca valisineria, that the female
had no fixed hours off the nest. Short rest periods during morning and
evening were regular, but the female also left at intervals during the day.
Departures became less frequent as incubation proceeded. All species
cover their eggs with down when they leave the nest.
The ruddy duck, Oxyura jamaicensis, represents the subfamily, Oxy-
ruinae. According to Low (1941), the nests are built by the female.
About eight eggs are laid, and the female may begin incubation before
the last egg is laid. The incubation period is 25 or 26 days. Although the
male does not incubate, he does not desert the female and aids in the
raising of the brood (Bent 1925). According to Friedmann (1932),
ruddy ducks deposit eggs in the nests of other species more frequently
than do other ducks and may be in the process of evolving a parasitic
nesting behavior pattern.
The behavior of Merginae is similar to that of other ducks. The 7 to 12
eggs are incubated by the female. Niethammer (1938) records the incu-
bation period as 31 to 32 days in Mergus serrator and M. merganser.
Weber (1946) gives it as 34 to 35 days in M. merganser. In M. serrator,
Torne (1940) found that on sunny days the female left the eggs between
0500 and 0600 hours, a short time about 0800 hours, and between 1100
and 1500 hours and again between 1800 and 1900 hours. On rainy days
she left for a half-hour at 0500 and again at 0900 hours and for an hour
at noon and at 1800 hours. The male accompanied the female during
these inattentive periods.
Summary. There are four types of nests (Delacour and Mayr 1945):
open nests on the ground, open nests raised above the ground on ledges
or stumps, concealed nests on the ground under rocks or in holes, and
nests located in tree hollows. One may suppose that originally the male
and female shared the duties of nest building, incubation, and care of
young, as in the Anhimidae, but in various groups the male has lost more
or less of his attentiveness. In the Cyginae and Anserinae, he does not
usually incubate; in the Oxyurinae and Merginae he is not concerned
with nest building either; in the Anatinae he is beginning to lose interest
also in the young birds after hatching, while in the Nyrocinae he com-
monly deserts the female during the incubation period. In his summary of
parental care in the ducks, Phillips (1922) states that in “nearly all
those species in which the female and the male have similar plumage
... the males are very pugnacious and active guardians of the family... .
There seems to be some rather important relation between the early
desertion of the females by the males and the presence of an eclipse
plumage... .”
The female restricts her inattentiveness to an hour or so in the early
morning and late afternoon and to occasional shorter periods during the
EVOLUTION OF PARENTAL CARE 189
day. In Nyroca she is alternately attentive and inattentive several times
throughout the day. Usually she covers the eggs with down on leaving
the nest, and commonly she is accompanied by the male on her inatten-
tive periods. Incubation does net usually begin until the set is complete.
ORDER: FALCONIFORMES
Of the living members of this order, there is no pertinent available in-
formation on attentive behavior in the superfamily Sagittarioidae, nor in
some of the subfamilies. There are two suborders.
Suborder: CATHARTAE; Family: CATHARTIDAE. Two eggs constitute a
normal set in the vultures, Cathartes and Coragyps, and these are laid
on consecutive days inside a hollow log or cave or on the ground in a
sheltered spot. Incubation begins with the second egg and lasts 39 to 56
days. The young stay in the nest or in its vicinity for 8 to 10 weeks. Both
parents take part in incubation and feeding the young. Coles (1944)
states that even when incubation is at its height, both birds may be simul-
taneously inattentive for periods in the morning and evening. E. S.
Thomas (Bent 1937) observed in Cathartes that there were 17 feeding
periods during nearly twelve hours of observation on one day.
Suborder: FALCONES; Superfamily: FALCONOIDEA; Family: ACCIPITRIDAE.
The family is divided into nine subfamilies. In the Elaninae, the white-
tailed kite, Elanus leucurus, has been intensively studied by Hawbecker
(1942). Nest building requires about 7 days, both sexes participating, and
at one nest the first egg was laid about 10 days after the nest was com-
pleted. Four eggs are laid on consecutive days, and incubation begins
with the first egg. Incubation lasts 30 to 32 days, and both sexes take part.
The male spends only a small share of time on the eggs, but he feeds the
incubating female. The young are brooded by the female, and at first
the male brings the food for both female and young, but when brooding
is no longer required the female also searches for food. The young leave
the nest in about a month but return to it for a time longer to be fed by
their parents.
The best study in the Perinae has been of the honey buzzard, Pernis
apivorus (Wendland 1935, Thiede 1938). Two eggs are laid nearly 2
weeks after the nest is ready; incubation begins with the first egg and
lasts 30 to 31 days. Both sexes share nest building and incubation about
equally; one attentive period of the male was at least three and a half
hours. The young are brooded about 3 weeks, at first about equally by
both sexes, but later more by the female. The young are fed wasp larvae,
at first by regurgitation, later from the bill. Green leafy twigs are brought
to the nest, and eggs or young may be covered with them during the
absence of the adult (Thiede and Zinkert 1932a, Gentz 1935). The nest-
ling period lasts 40 to 46 days.
190 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
In the kites, Ictinia misissippiensis (Sutton 1939) and Milvus migrans
(Schuster 1936a) of the subfamily, Milvinae, both sexes share the incu-
bation of the one or two eggs, although the male’s share is irregular and
sometimes questionable. Observations on M. migrans gave one complete
attentive period of nine hours for the female and eleven hours for the
male. In M. milvus (Niethammer 1938) the three eggs may be incu-
bated entirely by the female, beginning with the first egg, and the male
may bring her food. The nestling period is 40 to 50 days. The male supplies
both the female and young with all their food during the first 14 days.
He is especially active during the early morning hours (Thiede and
Zankert 1935). Skutch (1947a) observed both adults feeding insects to
one young Ictinia plumbea. The feeding rate was very irregular, depend-
ing on the weather, but averaged 2.4 times per hour. This high rate is
doubtless correlated with the type of food that is used.
In the European species of Accipiter of the subfamily Accipitrinae,
the female is chiefly responsible for nest building and incubation, al-
though the male may sometimes help. In A. nisus, Bal (1950) states that
the ratio of the female to the male in nest-building activities is 9 to 1.
In A. gentilis the male may relieve the incubating female four times
daily (Niethammer 1938) for periods of one to two hours (Siewert
1933). The two to four or sometimes six eggs are laid at intervals of 2
or more days and incubated for 5 to 512 weeks. Incubation begins before
the set is complete. The nestling period is from 4 to 6% weeks. The male
brings most of the food for the young at first, but later the female also
helps. In A. nisus, the male also feeds the incubating female who per-
forms this duty alone (Siewert 1930). In this species, L. Tinbergen
(1946) found an increase in number of trips to the nest with food from
2.1 per day when the young were 2 and 3 weeks old to 9.8 per day when
they were 10 weeks old.
In the subfamily, Buteoninae, both sexes usually share in nest build-
ing, incubation, and care of young (Bent 1937). Two eggs per set are
common, laid at intervals of 2, 4, or more days. Incubation begins with the
first egg and in the smaller species lasts 28 days. In the eagle, Haliaeetus
leucocephalus (Herrick 1934), it is 35 days and in Aquila verreauxii
(Rowe 1947) and in A. chrysaétos and A. pomarina (Niethammer 1938 )
it may be as long as 43 or 44 days. In A. verreauxti and H. leucocephalus
the attentive periods are from one to three hours long. However, in H.
albicilla, Schuster (1935) found the female incubating overnight until
0540 hours, the male on then until 0956 hours, after which the female
stayed on the rest of the day. During an all-day watch at a nest of
B. buteo, the male relieved the female twice for periods averaging about
four hours each. In A. chrysaétos, A. pomarina (Siewert 1932), Aquila
(Hieradetus) fasciata (Rivoire and Hue 1949), and in Buteo jamaicensis
EVOLUTION OF PARENTAL CARE 191
‘vorealis) and probably B. lineatus, the female takes much the greater
share of the incubation duties but is brought part of her food by the
male. In nearly 43 hours observation at a nest with two young A. chry-
saétos, food was brought five times by the female and seven times by
male or at the rate of 0.3 per hour (H. A. Gilbert 1934). Stewart (1943)
found the female alone feeding a brood of three B. lineatus which she
did at intervals of one hour. In H. leucocephalus the average rate is 2.5
to 4 times per day, most usually before 0900 and after 1500 hours. Rowe
(1947) records in A. verreauxii that during two different years a single
nestling, 3 to 9 days old, was fed at rates of 0.47 and 0.33 per hour. Young
eagles often stay in the nest 8 to 13 weeks, but in the smaller hawks the
time may be reduced to 6 weeks.
In the marsh hawk, Circus cyaneus (hudsonius), of the subfamily
Circinae, the female takes the greater share of nesting duties. Brecken-
ridge (1935) found only the female incubating and brooding, although
the male brought the young the greater part of their food. Other obser-
vers indicate that the male may occasionally incubate. He gives the incu-
buation period as 30 to 32 days. Witherby et al. (1939) and Haas (1939)
record that in C. pygargus and C. cyaneus the incubating female is fed
by the male. This takes place in the air away from the nest. The three or
five eggs are laid at intervals of 2 or 3 days; incubation begins before the
set is complete and it lasts 28 to 30 days. The nestling period is 5 weeks
or longer. Hennings (1936) spent 73 hours observing the growth of five
young in the nest, and during this time they were fed 77 mice and birds
or at the rate of 1.1 per hour. Claudon (1935) observed only the male
C. pygargus bringing food for the young. This he did at the rate of 1.1
per hour, when the young were small, but at the rate of 4.0 per hour
toward the end of nest life. Thiede and Zankert (1932b) observed four
young C. aeruginosus fed about 0.6 times per hour by both sexes during
the last 14 days of nest life.
In the subfamily, Circaétinae, Niethammer (1938) states that Circaé-
tus gallicus lays one egg. The male relieves the incubating female one or
two times daily, but she is chiefly responsible for incubation. The incuba-
tion period is 35 days and the nestling period very long, 9 to 11.5 weeks.
The male may bring food to the nest for the young four times daily.
Moreau (1945) found that one young Terathopius ecaudatus required
nearly 19 weeks to fledge. When it was one month old, it was fed once
every eight hours; during its last week in the nest it was fed three times
as frequently. Only one adult was concerned in caring for this young.
The Pandioninae is represented by the osprey, Pandion haliaétus. Both
sexes participate in nest building. The male may take an occasional turn
on the nest, but for the most part the female is responsible for the incu-
bation duties, during which time she is brought food by the male. The
192 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
two or three eggs may require as long as 35 to 38 days to hatch, and
the young may remain in the nest for over 7 weeks (Siewert 1941). The
male brings most of the food for the young which is fed to them at first
by the female. Later both sexes bring food at a rate of two or three times
a day (Bent 1937, Niethammer 1938 ).
Family: FALCON1DAE. In the subfamily, Polyborinae, Bent (1937) gives
the incubation period of Audubon’s caracara, Polyborus cheriway, as 28
days with both sexes sharing the duty.
In the Falconinae (Bent 1937, 1938, Witherby et al. 1939, Lawrence
1949b ) three or four eggs are commonly laid at intervals of 2 or 3 days.
In Falco cenchroides, however, Sharland (1931) observed that five eggs
were laid in 6 days. Groebbels (1937) records that both sexes are in-
volved in nest building in Falco subbuteo and F. tinnunculus. Incubation
begins before the set is complete, lasts 28 to 31 days (Niethammer 1938 ),
and is performed chiefly by the female. The nestling period commonly
varies between 25 and 35 days (Niethammer ). The male may take some
part in incubation in Falco subbuteo (D. Nethersole-Thompson 1931),
F. peregrinus, F. columbarius, F. vespertinus, F. naumanni, and F. tinnun-
culus (Groebbels 1937), but usually he is more concerned in supplying
the incubating female with food. In F. peregrinus, he starts feeding the
female during the laying period, alternates with her on the eggs at half-
hour to five-hour intervals, takes some part in brooding, and feeds the
female and the young again after hatching occurs (Schuster 193la, 1932a,
Gugg 1933, Demandt 1939, 1940). Labitte, Languetif, and Debu (1950)
believe that in this species incubation does not start until the set is
complete. In most species the male brings most of the food for the fe-
male and the young after hatching, and not until brooding is no longer
needed does the female help in hunting food for the young (Beebe
1950). In F. tinnunculus, the male brought food to the incubating fe-
male about once every 2 hours 13 minutes, but when there were young
he brought food once every 1 hour 24 minutes. Variation in number of
young from two to four did not affect the feeding rate, but the tempo of
feeding increased as the young got older. The female often left the eggs
to get food from the male, and during these periods the male would
sometimes cover them. The female brooded the young 7 to 10 days, and
the young left when 28 to 32 days old (L. Tinbergen 1940). In observa-
tions that extended throughout the nestling life of F. swbbuteo, Schuyl,
Tinbergen, and Tinbergen (1936) found that when only insects were
brought, both adults fed the young at the rate of 5.8 times per hour, but
when larger prey, as small birds and mammals, were also brought, the
rate decreased to about 1.2 per hour. The male fed insects directly to
the young, but often gave larger prey to the female who then fed the
young. Scholze (1933) did not observe any insects brought to the young,
EVOLUTION OF PARENTAL CARE 193
but birds were fed to them at intervals of two and a half to three hours.
Summary. Both sexes may participate in building the nest, incubat-
ing, and caring for the young. When both sexes incubate they commonly
alternate in shifts of three to four hours, but in certain species there is
only a single attentive period for each sex per day. The evolutionary
trend is for the female to assume an increasing share of incubating and
brooding and for the male to keep her supplied with food. Incubation
usually begins before the set is complete, often with the first egg. The
incubation period is commonly about 4 weeks long and the nestling
period somewhat longer, in some species it is considerably longer. After
hatching, the male commonly brings all the food to the female who
takes what she needs and feeds the young. After the young become 2
or 3 weeks old, the female decreases her brooding and takes her turn at
searching for food. Both sexes may then feed the young directly.
ORDER: GALLIFORMES
There are two suborders: Galli and Opisthocomi. Very little informa-
tion on attentive behavior is available for the latter group. Of the Galli,
no data are available for the family Numididae.
Suborder: Gatu, Superfamily: cracomweEa; Family: MEGAPopIDAE. The
artificial incubation of their eggs practiced by the megapodes in this
family is well known (Mayr 1930, Barrett and Crandall 1931). In Alec-
tura lathami studied in the Melbourne Zoo, Fleay (1937) states that a
mound of decaying vegetable material was built by the male. During
rains the mound was opened at the top and a crater made to catch the
water. The temperature of the mound varied between 29° and 35° C.
Both the male and female appeared to test the temperature by digging
a hole in the mound and inserting their heads. The male tolerated the
female near the mound only while the eggs were being laid. The first
egg was laid 18 days after the mound was started. The eggs were laid
in depressions, 18 to 19 inches deep. A total of 18 to 24 eggs was laid,
2 or 3 days apart, with their small ends down. The incubation period
was 9 to 10 weeks. The young birds hatched in an advanced stage and
were able to flutter up into trees upon emerging from the mound. The
male aided the young bird to escape by digging a hole in the mound
where the chick was scratching its way out. Delacour (1935) has also
compiled considerable information on this species.
According to Ashby (1922) and F. Lewis (1939, 1940), Leipoa ocel-
lata builds its mound in the sun. The nest is composed of sticks and
leaves mixed with sand. One or the other adult visits the mound daily,
opening it up on sunny days and closing it on cool days so that heat is
supplied partly by decaying vegetation, partly by solar radiation, and
partly by the heated sand. The usual set of 10 eggs is laid in 18 to 20
194 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
days and requires at least 57 days to hatch. The young chick may re-
quire two hours to escape from the mound and is not assisted by the
adults.
Pycraft (1910) records some mounds of very large size in other species,
which may be the accumulation of several years’ work or of more than
one pair. He also described another type of incubator for Macrocephalon
(Megacephalum) maleo in the use of burrows near hot springs or in
black volcanic sand that absorbs solar radiation very readily. Eulipoa
wallacei, Megapodius eremita (brenckleyi), and M. pritchardii have sim-
ilar habits. Pockley (1937) and Sibley (1946) have described how M.
eremita and M. freycinet use burrows in the side of active voleanos where
the soil at one to three feet depth is noticeably warmer than at the
surface.
It appears then that the birds in this family have lost their incubating
and brooding behavior and have become specialized in the use of arti-
ficial incubation of various sorts: heat of decomposition of decaying vege-
tation, solar radiation, soil heated by volcanic action or hot springs.
Armstrong (1947:42) makes the suggestion that artificial incubation
evolved in this group out of the habit of throwing leaves and other
debris over the eggs to conceal them when the adult bird left the nest
unattended. This decaying humus from the moist tropical forest floor
would have kept the eggs warm and been an aid to their incubation.
E. Ashby (1922) believes that solar radiation was forced upon some
species as a source of heat when the climate changed from a humid one
that permitted development of a lush vegetation to a dry one that elimi-
nated the obtaining of heat from decaying vegetation.
Family: cracmar. Bent (1932) has summarized information on the
chachalaca, Ortalis vetula. A small frail nest of sticks and leaves is built
by both male and female at heights of four to ten feet in bushes and trees.
Three eggs are laid, incubation lasts 22 to 24 days and is probably per-
formed by the female alone. The young are precocial and leave the nest
as soon as their down is dry.
Superfamily: PHASIANOIDEA; Family: TETRAONIDAE. Detailed accounts
of nesting of ruffed grouse, Bonasa umbellus, are available (Bump et al.
1947, Edminster 1947). Nest building is by the female. The nests are
merely hollows in the ground lined with whatever materials are avail-
able. There is then an interval of about a week before the first egg is
laid. An average ]l-egg set requires about 17 days for laying. Incuba-
tion is about 24 days and is performed entirely by the female. It does not
begin until the last egg is laid, so all hatch about the same time. The
female sits constantly except for 20- to 30-minute inattentive periods
twice a day. These periods have been observed between 0400 and 0500,
at 0950, at 1347, and between 1700 and 2000 hours. The early morning
EVOLUTION OF PARENTAL CARE 195
and evening hours are most characteristic. After hatching, the precocial
young continue to be brooded and fed by the female alone. This lack
of attentiveness by the male is also characteristic of Dendragapus ob-
scurus (fuliginosus) and Canachites canadensis (Bent 1932). Walkinshaw
1948b ) observed one inattentive period of a female off her eggs between
2043 and 2106 hours in the latter species.
Attentive behavior is similar in the ptarmigans, Lagopus lagopus and
L. mutus (rupestris), in that the female does the major share of the work
(Bent 1932), but the male guards the nest and young. Six to 12 eggs are
laid. Nethersole-Thompson (1939) found in L. scoticus that incubation
began with the next to last egg, lasted 23 days, and was performed by
the female alone. The hen left the eggs three times during one day at
intervals of six hours for inattentive periods of 45 to 60 minutes. The
young stay in the nest only a few hours and begin to fly within 14 days.
The male guards the nest and young but otherwise takes little part in
their care.
In Tympanuchus cupido and Pedioecetes phasianellus, the male takes
no part in nesting duties after the eggs are laid (A. O. Gross 1930, C. W.
Schwartz 1944, Lehmann 1941, Grinnell, Bryant, and Storer 1918). Leh-
mann (1941) states that the female prairie chicken may dispense with
her early morning inattentive period when incubation becomes advanced.
The young are brooded much of the time until they are a week old
but in decreasing amounts thereafter. Centrocercus urophasianus lays
a set of only seven eggs on the average, one egg being laid each day.
The incubation period is a little shorter, 20 to 22 days, and the female
is not assisted by the male in any phase of the nesting cycle. At one nest
the female was regularly inattentive during incubation between 0930
and 1130 and again between 1400 and 1500 hours during 5 days of ob-
servation (Girard 1937, Rasmussen and Griner 1938). Other European
species described by Niethammer (1942) have very similar behavior
to those forms specifically mentioned.
Family: pHASIANIDAE. The attentive behavior of the various quail in
the subfamily, Odontophorinae, is based essentially on the same pattern.
There have been detailed studies of several species: Colinus virginianus
(Stoddard 1931, Klimstra 1950), Lophortyx californica (Sumner 1935,
Glading 1938), L. gambelii (Gorsuch 1934), and Odontophorus guja-
nensis (Skutch 1947b). In the bobwhite, C. virginianus, nest building is
normally by the male. Incubation lasts 23 days and is performed either
by the male or by the female, more frequently by the latter, and the
two may very rarely alternate at this duty. During early incubation, an
inattentive period may be taken by the incubating bird both during early
morning and late afternoon, but later only one period is normally taken,
usually in the afternoon, and varies in length from one to nine hours
196 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
depending on the weather. The 14 to 15 eggs hatch within an hour,
indicating that incubation begins with the last egg. Both adults brood
considerably during the first 2 weeks and direct the feeding of the
precocial young. The main feeding periods are early and late in the day.
Observations on Alectoris, quoted by Stresemann (1928) and Nie-
thammer (1942), indicate that the female lays two sets of 8 to 12 eggs
in different nests. The male incubates and cares for the young at one
nest, the female at the other. The incubation period is 24 days. Both
sexes share incubation in Mearns’s quail, Cyrtonyx montezumae (Bent
1932), but it is uncertain whether the male takes full responsibility for
a nest.
Both male and female participate in nest building in L. californica
with the female taking the lead. Twenty-two days are spent in incubation
with the female on the eggs all the time except for a short period before
0830 and for a somewhat longer period, sometimes several hours, after
1530 hours. Workman (1943) cites a case where the male performed all
the duties of incubation when the female deserted after the set was com-
plete. Brooding is carried on by the female. The male accompanies the
female during her inattentive periods and after the hatching of the
young.
Incubation in L. gambelii requires 21 to 23 days and is performed by
the female. The male may assume these duties if the female is killed.
Gambel quail normally take two inattentive periods each day, one in the
morning and one in late afternoon or evening. These are from one to two
hours duration, or longer in hot weather. Hatching occurs in a few hours,
and the young are brooded during the first week. The male remains
near the nest and, after hatching, accompanies and guards the female
and brood.
Odontophorus is of tropical distribution and has some variations in
nesting activities. Only 4 eggs are laid instead of 12 to 16 found in north
temperate species. Likewise in Odontophorus several days may elapse
between successive eggs. In other quail, days may be skipped, but many
eggs are laid on successive days. Incubation is 24 to 28 days by the
female only. There is only one inattentive period per day, in the early
morning when the female is called off the nest by the male, but it may
last one and a half to three hours. All hatching occurs within 22 hours,
and the young birds are accompanied away by both male and female.
Beebe (1936) states that nesting behavior of pheasants in the sub-
family Phasianinae is essentially similar to that of other gallinaceous
species. Incubation lasts from 3 weeks to a month in different species.
The males do not share in nesting duties except to stand guard over
the female and young; particularly males with brilliant plumage never
EVOLUTION OF PARENTAL CARE 197
go near the nest. Kozlowa (1947) found the inattentive periods of the
incubating female ring-necked pheasant, Phasianus colchicus, to come
shortly after sunrise to about 0900 and again from 1800 to 2030 hours.
In Perdix perdix the incubating female has two regular inattentive
periods, in early morning and late afternoon, and may leave for short
intervals during the day. As incubation proceeds, she leaves the eggs
for shorter periods. The male guards the nest and helps to direct the
activities of the brood after hatching (Yeatter 1934, Yocum 1943, Nagel
1945, McCabe and Hawkins 1946). Goodwin (1948) found in captive
golden pheasants, Chrysolophus pictus, that the female sat almost mo-
tionless on the eggs without leaving for food or rest throughout the
period of incubation.
Family: MELEAGRIDIDAE. The female turkey, Meleagris gallopavo, re-
quires 28 days to hatch her clutch of 9 to 15 eggs. Egg-laying may be
somewhat irregular and incubation begins slowly, yet all eggs hatch
within 24 to 36 hours. The female does all the nest building, incubating,
brooding, and caring for the young. The male may call the female oft
the nest at first for feeding periods but later loses interest in her. He
has been accused of destroying the eggs of any nest that he may find.
Occasionally two or even three hens may lay in the same nest and
simultaneously incubate a large number of eggs. The females leave the
eggs for a short interval in the morning for feeding and possibly again
at midday for water, but toward the end of the incubation period they
may sit steadily without leaving at all during the day. Brooding during
the day may persist for 2 weeks after hatching, especially in rainy
weather and in early mornings, as the young are very sensitive to exposure
and wetting (Blakey 1937, Mosby and Handley 1943).
Suborder: opistHocomi; Family: opistHocoMiIDAE. Beebe (1909) states
that both sexes of the hoatzin, Opisthocomus hoazin, participate in the
building of the nest. Usually two eggs are laid per set. Apparently the
species is not polygamous.
Summary. The basic behavior pattern in this order is for the female
to do all the nesting duties alone. The male stands guard but seldom gives
any help. In Colinus, Alectoris, and possibly Cyrtonyx he has retained
more attentiveness than in other species, in that he often takes responsi-
bility for incubation and rearing a brood, but this is exceptional. The in-
cubating bird sits steadily from the time that the set is complete but
has one and often two inattentive periods per day, in the early morning
and in late afternoon or evening. The Megapodiidae are remarkable in
having evolved a very specialized type of behavior involving artificial
incubation. This results in increased development of the chick in the
egg so that it is exceptionally precocious at the time of hatching.
198 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
ORDER: GRUIFORMES
There are eight living suborders in this diversified order, but very
few species have been subjected to detailed studies of their nesting be-
havior. No information on attentive behavior has been found for the
suborders Heliornithes and Cariamae, or for the families Aramidae and
Psophiidae.
Suborder: MESOENATIDES; Family: MESOENATIDAE. Rand (1951) found
in Monias benschi a preponderance of males and the males performing
the duties of incubation and care of young. However, in Mesoenas, only
the female is known to incubate.
Suborder: turRNicEs; Families: TURNICIDAE, PEDIONOMIDAE. In the bus-
tards or hemipodes, the more brightly colored and larger sex is the fe-
male. The duller male performs the duties of incubation and caring for
the young. Four eggs are laid in a grass-lined depression in the ground
that serves as a nest. The young are precocial (Knowlton 1909). Groeb-
bels (1937) records that in Turnix sylvatica the female may incubate a
little during the first few days and that both sexes are concerned in nest
building. Seth-Smith (1907) found in his aviary that the male T. varia
and the male T. tanki alone incubated and cared for the young. The in-
cubation periods were 13 and 12 days, respectively.
Suborder: Grures; Superfamily: GRuomeEA; Family: GRumAE. Walkinshaw
(1947) studied the sandhill crane, Grus antigone, in captivity. Both the
male and female were concerned in nest building, which required 1 to 3
days. Two eggs were laid, and incubation lasted about 32 days. Both
adults incubate during the day with attentive periods about 44 minutes
long. The female sits on the eggs at night. The young are able to fly
when four months old but continue to be fed by the parents for six
months. In Grus canadensis, Walkinshaw (1949, 1950) states that the two
eggs are laid two days apart and that the incubation period is 28 to 30
days. Ten attentive periods on the eggs by both sexes averaged 165 min-
utes long but varied between 10 and 384 minutes in length. In another re-
lated species, Grus (Megalornis) grus, Witherby et al. (1938) state that
the two eggs are also laid at intervals of 2 days or longer; incubation
begins with the first egg, is 29 or more days long, and is shared by both
sexes. According to Niethammer (1942), the eggs are apparently resis-
tant to cold and may be left uncovered for several hours by the adults.
Schuster (1931b) found either the male or the female may incubate at
night. The young leave the nest in a few days and are able to fly in
9 to 10 weeks. During 2 full days of observation the average attentive
period of the male was 94 minutes and of the female, 69 minutes.
Christoleit (1939) has also made an intensive study of this species.
Superfamily: RALLOWEA; Family: RALLIDAE. The nest is often a platform
EVOLUTION OF PARENTAL CARE 199
or clump of marsh vegetation on which 6 to 12 eggs are commonly de-
posited at the rate of one per day. Skutch informs me that three or
four eggs are common in tropical rails, that the nest in Laterallus is
oven-shaped, while in Aramides the nest is a bulky basket high up in
a tangle of vines. Incubation sometimes begins before the set is com-
plete so that hatching may extend over several days, or the onset of full
incubation may be delayed until the set is nearly or quite complete.
One adult may care for the young as they hatch while the other con-
tinues incubation. The incubation period of the various species is com-
monly 19 to 21 days. The young leave the nest as soon as they hatch
and dry off. Both sexes incubate and care for the young, except in
Crex crex and Rallus aquaticus where the female does most or all of
the incubation and is fed on the nest by the male (Bent 1926, Witherby
et al. 1938, Walkinshaw 1937b, 1940, Ruthke 1939, Sooter 1942). With
Laterallus leucopyrrhus in captivity, Meise (1934) observed three eggs
laid on alternate days with incubation beginning with the last egg. Both
adults were on the nest at night, but after hatching, the female brooded
during the day and the male at night. The male feeds the female on
the nest, but the female may also leave occasionally to get her own food.
In the gallinule, Gallinula chloropus, both sexes have been observed to
share in nest building, and extra sleeping nests are sometimes made
for the young (Steinbacher 1939). According to Holstein (1938), the
male of this species is the principal nest builder and occasionally feeds
his incubating mate. Howard (1940) observed the male and female re-
lieving each other on the eggs at intervals of about 38 minutes. There
appears to be no essential differences between the three subfamilies
sometimes recognized.
Suborder: RHYNOCHETI; Family: RHYNOCHETIDAE. Knowlton (1909) re-
ports that in captivity both male and female kagu, Rhynochetos jubatus,
share in nest building and incubation, and that the incubation period
is 36 days.
Suborder: EuRYPYGAE; Family: EURYPYGmAE. According to Riggs
(1948), this family of sun-bitterns contains a single species, Eurypyga
helias, which inhabits dense tropical forests. The birds are not gregarious.
The nest is sometimes on the ground but may often be placed several
feet above ground in trees. Both sexes build the nest and take turns at
incubating the two eggs. The incubation period was 27 days in one nest
recorded in captivity, and the young bird stayed in the nest for 21 days,
and was fed by both parents. This long nestling period is unusual, as
the young birds are covered with natal down as in precocial species.
Suborder: ores; Family: ormae. In the bustards, Otis tarda, O. tetrax,
nests are placed in grassy fields, two to four eggs are laid, incuba-
tion begins with the last egg and lasts 20 to 28 days, and the female
200 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
alone incubates. The female is also responsible for the care of the pre-
cocial young which begin to fly after 5 or 6 weeks (Witherby et al. 1940,
Niethammer 1942).
Summary. The basic behavior pattern is for both sexes to share in all
the duties of nesting. A nest is built, a variable number of eggs is laid,
and the young are precocial. The Otidae show evolution in one direction,
i.e., the female takes over the preponderant or total duties of incubating
and rearing young, and the Turnices show it in the other direction in
that the male assumes these responsibilities.
ORDER: CHARADRIIFORMES
This is a large and varied order. The Charadrii is especially complex,
having seven superfamilies, twelve living families, and several sub-
families. No information is available on the superfamilies of Dromadoi-
dea and Thinocoroidea, each one of which has a single family.
Suborder: cHaRApRuU; Superfamily: JAcANOIDEA; Family: JACANIDAE. In
Jacana spinosa, A. H. Miller (193lb) found the role of the sexes re-
versed to the extent that the female was decidedly active in courtship
and the male performed most if not all of the incubation and care of the
young. Sets usually consist of four eggs. According to Hoffmann (1949),
the female Hydrophasianus chirurgus is polyandrous, laying seven to
ten sets of four eggs per year. The male begins incubation with the first
egg and performs these duties alone, and also the care of the young.
He may raise two broods per season. Incubation lasts 22 to 24 days;
the young are precocial and are tended by the male at least 2 weeks
after leaving the nest. During 14 observation periods coming at various
times of day, the male sat on the eggs only 52 per cent of the time,
although on one cool rainy day this percentage was raised to 82. The
female is vigorous in defense of the territory.
Superfamily: CHARADRIOIDEA; Family: ROSTRATULIDAE. In the painted
snipes, the female is the more brightly colored of the sexes and the roles
of the sexes are, in many ways, reversed. There is some evidence for
polyandry in this group (Pitman 1912).
Family: HAEMATOPODIDAE. E. J. M. Buxton (1939) states that nest
material continues to be added by the oyster-catcher, Haematopus ostra-
legus, after egg-laying starts. Webster (1941) found the eggs to be laid
at intervals of 1 to 3 days. Keighley and Buxton (1948) found incuba-
tion to start usually with the last of a two- to four-egg set. They give
the incubation period as 26 to 27 days, but in other species it may be
shorter. Both sexes incubate; Buxton states that the male does so for
shorter periods than the female. Webster believes that the adults change
places every 12 hours at the time of low tide and that this regime con-
tinues as they care for the young. Webster found considerable brood-
EVOLUTION OF PARENTAL CARE 901
—_
ing of the young during the first week after hatching, but only during
rainy weather for the next 2 weeks, and none thereafter. The young are
precocial and leave the nest in a few hours after hatching. Webster states
“one parent stands guard and feeds himself while the other feeds the
chick (and, probably, eats a little); then they change off at the turn
of the tide and the second parent stands watch or eats while the first
feeds the chick.” Dircksen (1932) states that both sexes care for the
young, but Buxton claims that the young are fed only by the male; the
female stops brooding to get food for herself but not for the young.
Family: CHARADRUDAE. Peters (1934) recognizes two subfamilies. In
the subfamily, Vanellinae, and in the lapwing, Vanellus vanellus, Laven
(1941) states that there are usually 30 to 45 hours between laying suc-
cessive eggs in the four-egg set. Niethammer (1942) gives the incuba-
tion period as 24 days. R. H. Brown (1926) found steady incubation to
begin with the last egg. Incubation is almost entirely by the female at
first, but the male takes some share later in the incubation period. The
young are precocial and able to fly when about 33 days old. The female,
and occasionally the male, broods frequently during the first 5 or 6 days
and during bad weather until the twelfth day. She broods the young at
night until the sixteenth day. Both adults feed the young.
The subfamily, Charadriinae, includes the several species of plovers.
In the killdeer, Charadrius (Oxyechus) vociferus (pp. 93-95), both sexes
share nest building, incubation, and care of young with probably the
male taking the greater share. Attentive periods during the 24 to 26
days of incubation averaged 33.6 minutes. At one of the two nests under
observation the incubating adult was a close sitter at night between
2000 or 2100 hours in the evening and 0500 or 0600 hours in the morning.
At the second nest, however, there was considerable nighttime activity.
The thermocouple record indicated continuation of daytime attentive
behavior until 2248 one night and its beginning at 0100 hours on another
night. This is of considerable interest since Spingarn (1934) records in
Charadrius hiaticula (semipalmatus) that the male and female alternate
on the eggs during both day and night at intervals ranging from 31
minutes to two hours 19 minutes. He believed that the male was the
more active of the two sexes in performing these duties. Ohlendorf’s
(1932) measurement of the length of attentive periods in this species
over three days averages 64 minutes. Laven (1940) states that the male
incubates at night and both sexes alternate during the day. Krésche
(1936) found the male doing the greater share of incubating in Chara-
drius dubius. Walkinshaw (1948a) timed two attentive periods of a male
black-bellied plover, Squatarola squatarola, at 35 and 30-++- minutes and
of a female at 65+ minutes. L. H. Brown (1948) found two or three
eggs per set in Charadrius (Afroxyechus) forbesi which were laid on
902, PARENTAL CARE AND ITS EVOLUTION IN BIRDS
alternate days. Both male and female incubated, brooded, and cared
for the young.
In other species of Charadriinae (Bent 1929, Witherby et al. 1940,
Niethammer 1942), three or four eggs make a complete set with the
eggs laid at one or two day intervals. The incubation period varies com-
monly from 23 to 28 days. Both sexes alternate at incubating the eggs
in varying proportions of time. In Eudromias morinellus, the male does
all of it; in Charadrius (Pagolla) wilsonia, the female is chiefly re-
sponsible.
The general tendency in this family, then, is for both sexes to share
the nesting duties with variation between species as to which takes the
major responsibility.
Family: scotopacipaE. In the subfamily, Tringinae, both sexes share
the incubation and brooding. The male apparently takes the major part
in Limosa limosa, L. lapponica, Tringa erythropus, Xenus cinereus,
Actitis macularia (Nelson 1930), A. hypoleucos (Niethammer 1942),
and Catoptrophorus semipalmatus (Wetmore 1921). In Numenius tenuir-
ostris, Tringa (Totanus) melanoleuca, T. ocrophus, and Heteroscelus
incanus, the female may do more than an equal share (Bent 1927, 1929;
Witherby et al. 1938).
In Arenariinae, the male surfbird does most if not all of the incubat-
ing in Aphriza virgata, although both sexes may tend the young (Bent
1929). In the turnstones, Arenaria interpres and A. melanocephala, both
sexes share incubation. In A. interpres, the four eggs are laid at intervals
of 15 to 80 hours, the incubation period is 23 to 27 days, incubation
begins with the third egg, and the female commonly incubates during
the day from sunrise until 1500 to 1700 hours while the male incubates
overnight (G. Bergman 1946).
In the subfamily, Scolopacinae, containing the woodcock and snipe,
the female does most of the incubation and brooding (Witherby et al.
1938, O. S. Pettingill 1936, Steinfatt 1938c). Steinfatt states that Scolopax
rusticola leaves the nest for 17 to 30 minutes in the early morning and
again in late evening in order to get food. Incubation begins with the
last egg and lasts 22 days. Rowan (1936) observed an unusual situ-
ation in the dowitcher, Limnodromus griseus, where only the female in-
cubated and only the male cared for the young.
In the Eroliinae, the male takes the greater share of incubation and
brooding in Erolia (Pisobia) bairdii, E. minutilla, Erolia (Calidris) tem-
minckii, and Eurynorhynchus pygmeus. On the other hand, the female
does so in Erolia (Pisobia) melanotes, E. fuscicollis (Sutton 1932), Tryn-
gites subruficollis, and Philomachus pugnax (Bent 1927, 1929; Witherby
et al. 1938). Swanberg (1945) found in the purple sandpiper, Erolia
(Calidris) maritima, that the attentive period was 15 hours long.
EVOLUTION OF PARENTAL CARE IO3
In this family, a nest of some sort is usually formed, which may be
a hollow in the ground, lined to a varying extent with dried grass or
other material. Four eggs are commonly laid, and the incubation period
is usually 20 or 24 days but may vary a few days either shorter or longer.
Either or both sexes may incubate. The young are precocious and com-
monly leave the nest a few hours after hatching. One or both adults will
care for the young.
Family: RECURVIROSTRIDAE. According to P. E. Brown (1949), both
sexes in the avocet, Recurvirostra avosetta, are involved in the building
of the nest and in incubation. The average of 55 attentive periods during
incubation was about 66 minutes, but there was considerable variation.
Often there was a ceremony of nest relief, but not always. Four eggs are
laid. The incubation period is 23 days and the young are prococial
within a few hours after hatching, but are brooded by one parent for
11 days. Yeates (1941) found the attentive periods on the eggs to be
very short in Himantopus himantopus, ranging from 5 to 15 minutes,
but these may not be normal.
Family: pHALAROPODIDAE. The reversed sexual dimorphism in this group
is well known. The female phalarope has the more colorful plumage and is
the more aggressive in courtship. The dull-colored males build the nest
and, after the eggs are laid, take over the major duties of incubation,
brooding, and caring for the young. Occasionally the female Phalaropus
fulicarius and Lobipes lobatus sit on the eggs, and they may share with
the male the care of the young. In Steganopus tricolor the male receives
no help from his mate. Nothing is known as to how the attentive periods
are regulated. Four eggs make up the usual set and the incubation period
has been variously estimated at 20 to 21 days (Bent 1927, Sutton 1932).
Superfamily: BURHINOIDEA; Family: BURHINIDAE. Bird (1933) states
that Burhinus oedicnemus lays two eggs on alternate days with incuba-
tion beginning with the second egg. Incubation lasts 26 to 27 days and is
shared by both sexes. The young leave the nest within a day after hatch-
ing. According to Banzhaf (1933), the male incubates during the middle
of the day and the female the rest of the time.
Superfamily: GLAREOLOWEA; Family: GLAREOLIDAE. According to
Witherby et al. (1938), Cursorius cursor lays two eggs which are incu-
bated by the female. In Glareola pratincola both sexes incubate the three
eggs (Yeates 1948). Groebbels (1937) gives a short incubation of 17
to 18 days. Stresemann (1928) records that Pluvianus aegyptius buries
its eggs 10 cm. in the sand and allows them to develop in the heat of
the sun. Moreau (1937b) describes how the male and female of Rhino-
ptilus africanus alternately shaded the egg, placed in full sunlight, at
intervals of about one hour during the day. At night the egg was incu-
bated in the ordinary way.
904 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
Superfamily: caHtontpoweEA; Family: cHtontiar. Murphy (1936) states
that Chionis alba may lay two or three eggs more than a week apart.
Incubation begins with the first egg to keep it from freezing. Conse-
quently the young hatch at so widely separated intervals that seldom
more than one survives.
Suborder: tart; Family: steRCORARUDAE. A simple nest is made by the
skuas, Catharacta skua, and jaegers, Stercorarius sp., often a mere hollow
in the tundra moss. Two eggs constitute a set with a possible interval of
two days between layings. Incubation is estimated at 23 to 26 days. Both
sexes share the duties of incubating and care of the young. The young
may leave the nest soon after hatching (Sutton 1932, Murphy 1936).
Family: LARwAE. The subfamily, Larinae, includes the gulls. Kirkman
(1937) found in the black-headed gull, Larus ridibundus, that the male
selected the nest site and began the nest building. Incubation began with
the first egg of the three-egg set and was shared by both sexes. The male
fed the female with regurgitated food from a month before nest building
until after the eggs hatched. Both adults fed the young.
According to the summaries of Bent (1921) and Witherby et al.
(1938), the general rule is for both adults to incubate about as soon
as the first egg is laid. The time that incubation starts varies, however,
with species, as Steinbacher (1938b) states that in L. argentatus incu-
bation does not begin until the last egg is laid. Both Goethe (1937) and
Kozlova (1938) found the female more attentive than the male in this
species. According to Kozlova, the female may sit on the eggs four to
five hours but the male for only a half-hour or less. The adults exchange
places six to eight times a day and several times during the night. Two
or three eggs are laid in a crude nest, often a day apart or more. Both
adults may be concerned in nest building. The incubation period is
variously estimated in different species of gulls at 20 to 26 days. After
hatching, the young may leave the nest as soon as they are dry, may
remain a few days, or may stay until fledged. Most commonly they leave
after a few days, when they no longer need frequent brooding. Both
adults feed and care for the young until fully fledged which may require
from 8 weeks (L. minutus) to 8 weeks (L. argentatus, Niethammer 1942).
The species nest in colonies on islands or along the shores of oceans
and lakes.
In the Sterninae, some little attention has been paid to the nesting
behavior of Sterna hirundo by Palmer (1941), Austin, Jr. (1932), Noll
(1943), and others. The male common tern scrapes out depressions in
the sand, and the female chooses one to complete as a nest. Usually three
eggs are laid at intervals of two days. The incubation period begins
with the first or second egg and lasts 21 to 23 days, and is participated in
by both sexes, with the female doing the major portion of it. Attentive
EVOLUTION OF PARENTAL CARE 205
periods may be 20 to 40 minutes but vary with the insolation and the
weather (Bent 1921). Huggins (1941) found that when exposed to a full
sun, tern eggs on a rocky island had a higher temperature when the
adult was absent than when the adult was present. Actually the chief
function of the adult’s attendance was to shade the eggs and prevent
their overheating. It may be that the adults are sufficiently sensitive to
the temperature of the egg and of the surroundings as to regulate the
length of their attentive periods accordingly. Marshall (1942) has re-
corded the regular desertion of their eggs at night by an entire colony
of terns, but this lapse of attentiveness is abnormal and was accompanied
by a high rate of nesting failures. Both adults feed the young which will
flee to the water at 12 days of age and can fly at 30 days.
In the noddy and sooty terns, Anoitis stolidus and Sterna fuscata, both
sexes take part in nest building, incubating, and feeding the young.
In Anotis the male and female relieve each other at intervals of 30 min-
utes to five hours, the average attentive period being about two hours.
The incubation period is 32 to 35 days. During the building of the nest,
sticks and other materials may be brought at the rate of three to six
times per hour. During this time, the male feeds the female at the nest,
but this ceases with the laying of the eggs and the assumption by the
adults of equal turns sitting on them. During the attentive periods the
bird may leave at intervals to drink and to wet the breast feathers which
may have some value in keeping the egg at the proper temperature. The
parent birds alternately feed the young at intervals of one to four hours
(J. B. Watson 1908).
In Sterna fuscata the attentive periods at incubating are much longer
as shifts are made at night, each bird remaining on the eggs for 24 hours
except for occasional short trips for water. Although the young may be
fed at any hour of day at intervals of four to seven hours, feeding is
most prevalent at dusk. The male may feed the female before the eggs
are laid but not afterward.
Behavior in other species of terns is essentially similar. Most species
are colonial. Bent (1921) records that in Sterna dougallii the attentive
periods of the roseate tern on the eggs were 40 to 60 minutes, with the
male’s periods shorter than the female’s. Witherby et al. (1938) state
that the bridled tern, Sterna anaethetus, may have 24-hour attentive
periods, with the shifts on the nest occurring at night as in S. fuscata. In
Chlidonias nigra, only the female incubates at night but both sexes alter-
nate during the day (Niethammer 1942). As a rule, eggs in this species
are laid at intervals of one day (Haverschmidt 1945). One adult has been
observed feeding the incubating bird in Chlidonias nigra, Thalasseus
(Sterna) sandvicensis, Sterna hirundo, Sterna albifrons, and Sterna fus-
cata. Usually the female is more attentive than the male. One to three
206 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
eggs make up the set, and these are laid on consecutive days or occasion-
ally at 2-day intervals. The incubation period varies from 20 (Haver-
schmidt 1945) to 26 days. The young leave the nest in a few days but
are fed by their parents until after they are able to fly. O. S. Pettingill
(1939) gives the feeding rate of the young in Sterna paradisaea as 2 to
12 times per hour.
Family: RYNCHOpIDAE. The nest of the black skimmer, Rynchops nigra,
is only an unlined depression in the sand or in the ground. There are
commonly four or five eggs in a set, and incubation is performed by the
female. Both sexes feed the precocious young. The length of the in-
cubation period appears to be unknown (Bent 1921).
Suborder: AuLcAE; Family: aucmar. Most species in the family breed
in colonies and have very little or no nest, although some of the puffins
and auklets dig burrows, at the ends of which they place their eggs.
Most species lay their single egg in rock crevices or on narrow ledges of
steep cliffs. The black guillemot, Cepphus grylle, commonly has two eggs
laid at intervals of 3 days, and incubation begins after the second egg is
laid (Winn 1950). The incubation period is variously given for dif-
ferent species as 3% to 5 weeks. In some of the auklets, the young enter
the water within 2 or 3 days, but in most other species, not for several
weeks after hatching, until they are at least half grown and partially
feathered, even though they may not yet be able to fly.
Both sexes dig the burrow, when one is prepared, and incubate the
eggs and care for the young. Observations indicate in Brachyramphus
(Endomychura) hypoleucus, Ptychoramphus aleuticus, Lunda cirrhata
(Bent 1919), and Cerorhinca monocerata Bailey (1927) that there are
two daily shifts at incubating, one in the evening and the other in the
early morning. The bird on at night would have the shorter shift due
to the long daylight hours of northern regions where these birds are
commonly found. There is some uncertain evidence that on his return,
the male may feed the female on the nest. Lockley (1934) made an inti-
mate study of Fratercula arctica, and found that only the female puffin
incubates, that she incubates chiefly at night with occasional attentive
periods during the day, that she leaves her burrow for feeding during
most of the day, that the incubation period is 40 to 43 days long,
that both parents feed the young and this feeding is most vigorous
at the two flood tides each day, and finally that the young are fed for
40 days until they become fat after which they are deserted and find
their own way out to the sea. The entire nestling period may be 47 to 51
days long.
Summary. The basic pattern of attentive behavior in Charadriiformes
is for a scant nest to be formed in slight hollows in the ground, in bur-
rows, in rock crevices, or on ledges of cliffs. One to four eggs are laid,
EVOLUTION OF PARENTAL CARE 207
usually at intervals of one to several days. Incubation often begins before
the set is complete and lasts 2% to 4 weeks or lonver. The young may
be precocial and leave the nest as soon as they are dry or they may stay
for several weeks. In the Laridae an intermediate condition occurs in
that the young may leave the nest soon after hatching but continue to
be fed by their parents until they become fledged. Both adults take turns
at incubating, brooding, and feeding the young. It is uncertain whether
the primitive behavior pattern during incubation involved long attentive
periods with only one or two shifts between adults per day as in the
oyster-catcher Haematopus ostralegus, purple sandpiper Erolia mari-
tima, turnstone Arenaria interpres, in the noddy, sooty, and bridled terns
Anoiis stolidus, Sterna fuscata, and S. anaethetus, and in most of the
Alcidae, or whether the attentive periods were shorter and came more
frequently as in other species. The birds are more active at night than
in many orders.
Superimposed on this basic pattern are two divergent trends in the
evolution of specialized behavior patterns. One trend is for the female
to assume an increasing proportion of the work, which is manifested
to a certain extent in several families but probably best developed in
some species of Scolopacidae and Sterninae. There are scattered refer-
ences of the male bringing food to his incubating mate. The other trend
is the reverse, in that the male assumes an increasing amount of the
work. This is evident in some Charadriidae, in several species of Scolo-
pacidae, in the Jacanidae, Rostratulidae, and Phalaropodidae.
ORDER: COLUMBIFORMES
Suborder: pTEROCLETES; Family: prERocLIDIDAE. Witherby et al. (1940)
state that in the Pallas sand grouse, Syrrhaptes paradoxus, the birds lay
three eggs and incubation is by both male and female. Niethammer
(1942) records the incubation period as 28 days. Groebbels (1937) states
that in two species of Pterocles the female incubates during the day and
the male at night and that the incubation period is 22 to 23 days. Bowen
(1927) differentiates between species that are diurnal and nocturnal.
Diurnal species come to drink with clock-like regularity between 0700
and 0900 hours, after which they go far out into the desert, to return
again about two hours before sunset. Other species do not come to their
watering places before sunset but often continue to come well into the
night and possibly also in the morning before sunrise. Seth-Smith (1907 )
recounts how adult Pterocles alchata soak their breast feathers with
water, fly back to their young in the nest who suck off the water to
supply their needs.
Suborder: coLuMBAE; Family: RaPpHAE. Knowlton (1909) quotes from
an early account of Francois Leguat in 1691 that the solitaire, Pezophaps
208 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
solitaria, laid but one egg, that both sexes incubated, that the incubation
period was 7 weeks, and that the young did not become independent for
several months.
Family: cotumprpak. There are four subfamilies of pigeons and doves
recognized, but nesting data are available for only the Columbinae. In-
formation concerning several other species is taken from Bent (1932),
Witherby et al. (1940), and Niethammer (1942); in addition more de-
tailed data were obtained on Columba fasciata from Neff and Niedrach
(1946); C. livia from Levi (1941) and Oskar and Kathe Heinroth
(1948); C. oenas from Steinfatt (1941a); Zenaidura macroura from Nice
(1923, 1938), McClure (1943), and Pearson and Moore (1939); Ec-
topistes migratorius from Brewster (1889), French (1919), and Mitchell
(1935); Zenaida (Melopelia) asiatica from Neff (1940); Columbigallina
passerina from D. J. Nicholson (1937), Scardafella inca from Heilfurth
(1934b) and Anderson and Anderson (1948); Streptopelia decaocto from
Keve (1944); and Oreopeleia montana from Skutch (1949b).
There is considerable uniformity in the behavior pattern of attentive-
ness in this subfamily. Both sexes share in nest building, but the female
does the major portion of arranging the materials. Normally only one or
two days are required to complete the nest but occasionally a week or
longer is taken. Usually two eggs are laid. In C. livia they are laid with
an intervening interval averaging 44 to 45 hours. In band-tailed pigeons,
C. fasciata, one-egg sets are more common than two-egg sets, and in
the passenger pigeon, E. migratorius, one-egg sets occurred frequently.
Stresemann (1933:760) states that the larger species lay one egg, others
two. Some incubation begins as soon as the first egg is laid, but at least
in C. livia and O. montana it is not continuous until the second egg
appears. E. migratorius was colonial in its nesting and was reported as
going many miles away from its nest to obtain food for itself and the
young (Brewster 1889).
Incubation is shared by both sexes in probably all species. Each sex
has one attentive period per day, the male is commonly on the eggs
from about 0930 to 1600 hours and the female the rest of the time,
although the exact time varies between species and individuals, and
from day to day. The male’s attentive period in S. inca is unusually short,
from 1100 to 1500 hours, but the female may break her long period on
the nest by a short period off in early morning and again in late after-
noon. Skutch (personal communication) observed in Guatemala that
the male white-winged dove, Z. asiatica, sat on the eggs from 0832 to
1715 hours. A day may be skipped occasionally in various species, so
that one bird remains on the eggs without relief. Goodwin (1947) records
a case in C. livia of the female incubating almost continuously through-
out the incubation period after the desertion of the male.
EVOLUTION OF PARENTAL CARE 209
The incubation period is commonly 16 to 19 days long in Columba,
14 days or a little longer in most other genera, but only 11 days in
Oreopeleia. This latter genus is also exceptional in the family and also
for a tropical species in having the nestling period only 10 days long.
The period that the young remain in the nest is commonly 12 to perhaps
18 days in other genera except for Columba where it is 27 to 35 days.
The young are brooded by both sexes, in much the same manner as
the eggs are incubated, for 7 to 15 days. They are fed with “pigeon milk”
by both sexes for the first week or more but are usually given solid food
before leaving the nest. The rate of feeding the young varies greatly.
Skutch found in O. montana that the young were fed 22 times when one
day old and only three times per day when they were a week old. How-
ever, they were fed more copiously as they grew older, and both nestlings
were fed on each visit. Only one nestling was fed at a time when they
were very young. In observations that extended from daylight to dark,
Neff and Niedrach (1946) reported that in C. fasciata the male fed the
young three times daily the first week and twice daily the second week.
The female did not feed the young until they were 20 days old, then each
sex fed them once per day.
Summary. The basic behavior pattern in this order is for both sexes
to share in all phases of the nesting duties, with each sex having one long
attentive period per day.
ORDER: PsITrACIFORMES
This is a large and varied order of parrots and their allies, but con-
taining only one family which is divided into six subfamilies. Very little
study has been made of their nesting behavior except in captivity.
Family: psrrraciak. In species of Agapornis the female does most
of the nest building. Incubation begins with the first egg and lasts 21
days, during which the male supplies the incubating female with food.
In A. pullaria, the male fed the incubating female only once or twice a
day (Hampe 1937a). The behavior of Loriculus is similar except the in-
cubation period is 17 to 21 days. Macgillivray (1927) and Hampe
(1937b, 1938, 1939, 1940, 1941, 1942) have made studies of Platycercus
eximius, P. icterotis, P. adscitus, Neophema bourkii, N. elegans, N.
chrysostomus, Psephotus varius, and P. haematonotus in captivity. These
species belong to the subfamily, Psittacinae, native in Australia. The birds
have a nest and lay three to six eggs in a set, usually on alternate days.
Incubation may begin before the set is complete and lasts 17 to 20 days;
the young are brooded for 7 to 12 days or longer and leave the nest at
the age of 28 to 36 days. The female incubates and broods almost con-
tinuously while being supplied with food by the male. Both adults bring
food to the young after they become older. In P. eximius and N. bourkii
I10 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
the female begins to feed herself when the young reach 8 days of age,
in P. adscitus not until they are 14 days old. The female will, however,
search for food for herself and her young during these first few days
if the male is killed or deserts. In the records compiled by Groebbels
(1937), the male supposedly takes some share of the incubation duties
in Nymphicus (Calopsittacus), Conuropsis, Agapornis, and Melopsittacus.
Large parrots may take 30 to 31 days for incubation (Heinroth 1924-33).
ORDER: CUCULIFORMES
There are two suborders of Cuculiformes but no information is avail-
able on the plantain-eaters, Musophagi, Musophagidae. The suborder,
Cuculi, contains but the one family.
Suborder: cucutt; Family: cucutmar. This family is a heterogeneous
one. Six subfamilies are recognized, and there is considerable differentia-
tion of behavior between them. No information is on hand for one
subfamily, Couinae.
The Cuculinae includes the European cuckoo, Cuculus canorus, and a
large number of oriental and African species that are parasitic (E. C. S.
Baker 1942, Friedmann 1949a, b). Cuculus is parasitic on a large variety
of small birds; Clamator often parasitizes species of Corvidae. No nest is
built, although the female Cuculus is sometimes seen carrying nest ma-
terial during the mating period (Chance 1922). An egg of the host species
is removed when the cuckoo lays its own. As many as 12 eggs are regu-
larly laid per season by Cuculus canorus, but this depends somewhat
on the number of available nests of the host species. Occasionally even
25 eggs are laid in one season. Eggs may be laid every other day. Incu-
bation requires 12 to 13 days, and the young bird remains in the nest 20
to 23 days. The young bird is continued to be fed for another 3 weeks
after leaving the nest.
In the subfamily, Phaenicophaeinae, the two species of Coccyzus
occurring in North America have essentially the same behavior (Table
42). A nest is built. Egg-laying is irregular, and incubation begins with
the first egg of the two to four that form the egg-set. As a result, hatching
extends over several days, and there may be young of different ages and
eggs in the nest at the same time. The two species frequently lay their
eggs in each other’s nests and occasionally in the nests of other species.
Social parasitism, as in Cuculus, has not, however, developed; in one nest
where both species had laid eggs, both were observed to incubate and
brood at different times (Allison, MS). Bent (1940) gives the incubation
period as 14 days; Spencer (1943) found two marked eggs to hatch in 10
and 11 days. Both sexes share in incubation and brooding with long
attentive periods. C. H. Johnson (1942) found an average brooding
period of 49.3 minutes throughout the nest life of young Coccyzus ameri-
EVOLUTION OF PARENTAL CARE 21]
canus. The nestling period is only about a week, at the end of which the
young leave the nest, still unable to fly, and enter into a climbing period.
During this period they scramble around through the bushes, and an-
other two weeks may lapse before they can fly (Herrick 1935). The feed-
ing rate is low. In addition to the records in Table 42, Herrick (1910a)
found an average of 1.0 times per hour for four young at one nest and
2.4 times per hour for 3.8 young at another nest. His observation covered
many hours over six different days at each nest.
In the Crotophaginae, studies of nesting behavior are available for
Guira guira and Crotophaga ani (Davis 1940a,b) and C. sulcirostris
(Bent 1940), the latter account based largely on observations by Skutch.
These birds have developed a remarkable communal behavior in terri-
torial defense, in having one nest used by several pairs, and in other
phases of nest life. Occasionally a single pair may have a nest to itself,
at least in G. guira and C. sulcirostris, but commonly two or three pairs
join together. Davis found some indication in C. ani that monogamy,
polygyny, and polyandry may all occur in different situations. Alvarez
(1948) actually observed in C. sulcirostris a male copulating repeatedly
with two different females. Both sexes of all pairs in a group aid in build-
ing the nest, usually the females arrange the materials that the males
bring to them, and they themselves may gather some material. In
C. ani the set laid by one female is commonly six eggs, in C. sulcirostris,
three or four, in G. guria, five to seven. Several females may lay in the
same nest, and all birds, both male and female, take turns at incuba-
tion. In C. ani and C. sulcirostris a single male incubates at night
(Skutch). Sometimes a female will lay eggs in a nest but not help to
incubate. Davis noted considerable irregularity in that different females
in a group would lay eggs at different times, sometimes eggs were laid
before the nest was ready so that they had to be deposited on the
ground. Incubation lasts 13 to 14 days. The young remain in the nest
for only 5 or 6 days, when they begin the climbing period also noted for
other cuculids. They are commonly brooded during the day for the
whole period in the nest and will also return to the nest at night dur-
ing the climbing period. Skutch noted in C. sulcirostris the longest atten-
tive periods during incubation at 30 to 60 minutes, and he observed the
young fed at the rate of 12 times per hour. Davis recorded the rate of
feeding the young in G. guira in two nests at 0.8 and 6.0 times per hour.
All of the adults of both sexes may participate in feeding the young.
The roadrunner, Geococcyx californianus, is in the subfamily, Neomor-
phinae. Its nesting behavior is not well known (Bryant 1916; Sutton, see
Bent 1940). A nest is built but the number of eggs varies between wide
limits, 2 to 12. Where large numbers of eggs occur, probably they are
laid by more than one female. The incubation period appears to be 18
919 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
days, which is long. Incubation begins with the first egg, and since the
eggs are deposited at intervals of several days, by the time the last young
hatches, the first young may be half the size of the adult. Bryant states
that both sexes incubate and care for the young, but Sutton cites some
evidence that only the female incubates. Sutton gives some observations
to indicate that, like Coccyzus, young roadrunners may leave the nest
after a week or so and have a climbing period before they become inde-
pendent of their parents. Peters (1940) classifies Tapera naevia also in
the Neomorphinae. However, this species has a pattern of behavior quite
different than Geococcyx in that it is parasitic on other species, more
nearly like the Cuculinae (Friedmann 1933).
In the Centropodinae, Spennemann (1928) believes that only the
male builds the nest, incubates, and feeds the young in Centropus ben-
galensis (javanicus).
Summary. One cannot give any general pattern of attentive behavior
in the Cuculidae that will fit all groups. The occurrence in several genera
and different subfamilies of a short nestling period, followed by a period
of climbing through the bushes and trees near the nest, is, however, of
special interest in this regard. Perhaps this behavior characteristic is
typical of the order as a whole, as Moreau (1938) reports similar behavior
also for species in the family Musophagidae, suborder Musophagi. Evolu-
tion of behavior has been relatively rapid in the Cuculidae. It would seem
that the behavior of the genus, Coccyzus, in the subfamily, Phaenico-
phaeinae, adheres most closely to an expected behavior pattern such as
is found in other orders. In this group both sexes participate in all phases
of nest life, which follows the usual sequence of courtship, nest building,
egg-laying, incubation, brooding, and feeding the young. However, two
irregularities may be noted in the behavior of Coccyzus. Eggs are laid at
intervals of 1 to 3 days and with incubation beginning with the first egg,
there are often considerable differences in the ages and development of
the young. In other words, the various phases of the reproductive cycle
are not as definitely defined as in other species. This may indicate a weak-
ness in the timing of the reproductive behavior pattern that, if present in
the ancestors of modern cuckoos, could have foreshadowed the evolu-
tion of the parasitic behavior. The other irregularity is the occasional
laying of eggs in the nests of other birds. When other species are con-
cerned, this would have forecast the development of parasitism; when
the eggs are laid in the nests of other cuckoos, either the same or related
species, and sometimes the joint care of them and the young, the first
beginning of a social reproductive behavior pattern would have been
suggested.
Friedmann (1933) believes that the cuckoo family is of ancient ori-
gin, probably in southern or southeastern Asia. Apparently the family
EVOLUTION OF PARENTAL CARE 213
branch that dispersed into the Americas did so before the parasitic be-
havior had become established as it later developed elsewhere over the
world. If this is true, then the parasitic behavior in Tapera of South and
Central America must represent an independent and convergent evolu-
tion. There is evidence in some species of parasitic cuckoos, that the
adult bird may still occasionally feed the young (Friedmann 1949a,
Moreau 1949b, Chisholm 1950).
Darwin (1859) long ago postulated the evolution of parasitism in
Cuculus from progenitors with behavior patterns like Coccyzus. He recog-
nized that the 2- or 3-day intervals between laying of the eggs and the
consequent diverse ages of the young birds in the nest was a handicap
for the raising of a full complement of vigorous and healthy offspring.
He postulated as a consequence that the occasional raising of young by
foster parents may have proved advantageous for the species and that
this directed an evolutionary trend in behavior until it became the sole
means of reproduction. Herrick (1935:105-6) seems to agree with Dar-
win when he states “. . . it seems to me probable that this lack of har-
mony between nest-making and egg-laying may be the ‘loosened screw
that makes the acquisition of such a habit possible.”
E. C. S. Baker’s (1942) ideas as to the origin of parasitism appear
conflicting. He believes that the first birds laid their eggs in various
places and that nest-building behavior evolved later in the various groups.
He states (p. 98): “. . . parasitism seems to have been acquired not by
birds which were originally nest-builders, but by those who had never
acquired the art of nest-building.” Later in this discussion, however, he
states (p. 99): “. . . our most primitive cuckoos are not parasitic, they
make their own nests, hatch their eggs and rear their young.” These
statements would seem to mean that parasitic and nonparasitic cuckoos
must have evolved independently from very early ancestors. We cannot
agree with this hypothesis.
D. Davis (1942b) is probably correct in stating that social nesting is
not a stage in the development of parasitism, but it is a distinct side
branch in the evolution of a peculiar nesting behavior. Note has already
been made how Coccyzus species may lay in each other’s nests and both
species care for the eggs and young in one nest. In Geococcyx, it is not
uncommon for several females to lay their eggs in one nest, but there is
no evidence available that the duties of incubation and raising the young
are shared by more than one pair. In Crotophaginae, D. Davis (1942b )
traces the phylogeny through three levels: I, Guira guira, H, Crotophaga
major, and III, C. ani and C. sulcirostris, with increasing specialization at
each level. He describes three primary factors conducive to the develop-
ment of social nesting behavior: a) breakdown of territorial defense by
individual pairs due to weak sexual fighting, lack of song, poorly devel-
914 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
oped courtship performances, and the appearance of composite terri-
torial defense by the colony; b) aberrant breeding behavior involving
only sporadic attentiveness to nest and eggs and young, lack of attune-
ment between egg-laying and nest building, and spontaneous ovulation
without complicated courtship; and c) type of habitat in that the birds
originally occurred in savannahs where they could scatter to feed but
they were compelled to concentrate in isolated groves of trees to roost
and nest. It would seem that here again, the loss of precise definition and
timing of the various phases in the reproductive cycle was prerequisite
for the evolving of a new type of attentive behavior.
Perhaps the aberrant behavior of Centropus bengalensis, where the
male asumes all the nesting duties, is still another evolutionary compen-
satory pattern for the loss of attentiveness. This species may indicate
that it was in the female rather than the male that the main disturbance
occurred in the reproductive cycle.
ORDER: STRIGIFORMES
This order contains two living families. Probably because of their
nocturnal habits, few detailed studies have been made of their attentive
behavior.
Family: ryrontwar. The barn owl, Tyto alba, nests in old buildings,
cliffs, trees, or walls. Often no nest is built or only a crude pile of sticks
or broken-up regurgitated pellets. There are commonly six or seven eggs
laid at intervals of 2 days (Wallace 1948); Niethammer (1938) gives
four to six eggs as the usual set. Incubation may begin soon after the
first egg is laid, as broods of young are obviously of different ages, de-
pending on time of hatching. Incubation time has been variously deter-
mined, but is probably 30 to 34 days (Wallace 1948, Witherby e¢ al.
1938). Forbush (1927) states that “the female while incubating is stead-
ily supplied with food by the male, but occasionally she leaves the nest,
and he takes her place thereon, and probably in some cases he assumes
some part of the duties of incubation, as both male and female have
been seen sitting side by side on the eggs.” Niethammer states that only
the female incubates. After hatching, the young remain at the nest site
about two months. Bussman (1935) attached a terragraph to a nest con-
taining four young. An average over several nights, when the weather
was clear, gave 11.3 feedings in an avera~e hunting period of 5 hr. 33
min. per night (2.0 per hour). In 1937 he obtained another record at a
nest with six young. Here he found the female doing the brooding for
10 to 11 days. Over 28 nights, food was brought to the young eight times
per night. Most observers agree that both parents share this duty.
Family: srricipAE. The best studies of the nesting behavior of owls
are those of Sherman (1911) and A. A. Allen (1924). on the screech owl,
EVOLUTION OF PARENTAL CARE 915
Otus asio; Gugg (1934) on the eagle owl, Bubo bubo, F. M. Baumgart-
ner (1938) on the great horned owl, Bubo virginianus; Sutton (1932) on
the snowy owl, Nyctea scandiaca (nyctea); Haverschmidt (1946) on the
little owl, Athene noctua; Hosking (1941) on the long-eared owl, Asio
otus; Kuhk (1943, 1949) on the Tengmalm owl, Aegolius (Cryptoglaux)
funereus; and Santee and Granfield (1939) on the saw-whet owl, Aego-
lius (Cryptoglaux) acadicus. Bent (1938), Niethammer (1938), and
Witherby et al. (1938) have summarized much miscellaneous informa-
tion.
Nests are not ordinarily built (Schuster 1930). Bubo virginianus, Strix
(Scotiaptex) nebulosa, and Asio otus (wilsonianus) utilize old hawk or
crow nests and in some areas may add more sticks; apparently in Bubo
this repair work is participated in by both sexes. Other species commonly
nest in natural cavities or old woodpecker holes; Spzotyto cunicularia
may enlarge an old prairie dog or ground squirrel burrow; Nyctea scan-
diaca and Asio flammeus nest in slight depressions made in ground vege-
tation. Usually there is little or no lining, but occasionally there are
feathers from the bird’s breast or, in Speotyto, dried chips of mammal
excreta.
The number of eggs per set varies from two to three in Bubo, Glauci-
dium, Micrathene (Micropallos), and Strix, to as many as seven or eight
in Nyctea and Speotyto. The eggs are laid at intervals of 2 days or
more, and incubation begins with the first or second egg.
Incubation and brooding in all species are done chiefly by the female.
There is considerable difference of opinion as to how much incubating
the male does, but in Bubo, Micrathene, Speotyto, Strix, and Asio flam-
meus he is supposed to take some part. In several genera, Otus, Nyctea,
Glaucidium, Athene, and Aegolius and in Asio otus (Niethammer 1938 )
and Bubo bubo (Gugg 1934), the male is largely responsible for sup-
plying the incubating female with food, so that she leaves the nest only
at infrequent intervals. In Aegolius funereus, the male feeds the female
four or five times in the night and the female leaves the nest for only
three to nine minutes in early morning. Fleay (1942) states that in Ninox
connivens the incubating female leaves for only a few minutes after
dusk to get food. It may well be that some reported cases of males’ incu-
bating may be based on these visits of the male to the nest with food for
his mate. After the young hatch, the male continues to supply the nest
with food, the female taking what she needs and passing on the rest to
the nestlings. Apparently it is only after the need for brooding is over
that the female searches for food for the young, so that, in general, her
role in this duty is a reduced one.
Bendire (1892) reports that the incubation period is only 2 weeks in
Micrathene, but this should be reinvestigated. It is commonly 3% to 4
216 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
weeks in other species or 5 weeks in Nyctea and Bubo. Brooding of the
young may last 2 to 3 weeks and the young commonly remain in the
nest for 3 to 5 weeks altogether.
A. A. Allen (1924) has seven nights’ observations of male and female
screech owls, Otus asio, feeding two young. Feeding periods lasted 6.0
to 7.5 hours each night, and the average feeding rate was 7.7 visits to the
nest per hour. Santee and Granfield (1939) have similar observations
of both adults feeding five young saw-whet owls, Aegolius (Cryptoglaux)
acadicus, over three nights when the young were 19, 25, and 28 days old.
The feeding periods were from 5.0 to 5.9 hours long, and the number of
visits to the nest averaged 1.1 per hour. Haverschmidt (1946) recorded
both adults of Athene noctua feeding two young, 16 to 23 days old, at the
rate of 7.0 times per hour, and feeding one young, 24 to 35 days old, at
the rate of 4.4 times per hour. During incubation he observed inattentive
periods of the female at all hours of the day and night, but after hatch-.
ing, the young were fed chiefly at night. Bussman (1931) recorded 21 to
48 comings and goings per day in this species, mostly at night but some
by daytime.
All genera mentioned above belong to the Buboninae except Strix,
Asio, and Aegolius which are placed in the Striginae. There appear to be
no differences in behavior between these subfamilies.
Summary. The basic pattern for the order as a whole is for the female
to sit nearly continuously on the eggs and the newly hatched young. The
male may occasionally take a turn, but his usual duty appears to be to
supply the female and young with food. Most species are nocturnal. In-
cubation in this order commonly begins with the laying of the first egg,
with the result that the young hatch at intervals and maintain a marked
difference in size through the nestling period.
ORDER: CAPRIMULGIFORMES
There are two suborders and five families in this order, but data are
available on only the one family.
Family: caprimutcwae. No nest is built. There are two eggs, and these
are laid on alternate days.
In the whip-poor-will (Table 42), only the attentive behavior of the
female is averaged for the incubation period. Raynor (1941) observed
the male on the eggs three times, between 2045 and 2325 hours, for
periods that averaged only eight minutes. Arnold (1937) believed only
the female incubated, and she observed absences of 15 to 25 minutes.
The female sits steadily on the eggs during the daylight hours, as this
species is largely nocturnal in its habits. Both adults feed the young at
night, and the male participates with the female in brooding them at this
time. The young have no true nestling period as they move from one
EVOLUTION OF PARENTAL CARE Ory
location to another at frequent intervals. The behavior of Caprimulgus
europaeus is similar (Lack 1932, Stiilcken and Briill 1938) except for
being more crepuscular. The male relieves the female on the eggs for 15
to 20 minutes in the evening and possibly also at dawn and participates
in brooding and feeding the young. The incubation period is given as
only 16 to 17 days and brooding as 16 to 20 days. The young begin to
fly at 16 days but remain dependent on the adults for food for 31 days or
longer. Both sexes take turns at incubating and brooding in the poor-will,
Phalaenoptilus nuttallii (Orr 1948).
In Nyctidromus albicollis, Skutch (Bent 1940) found the male and
female taking turns on the eggs and brooding the young, relieving each
other every two or three hours during the day. At night only the female
covered the eggs.
Although there are some records of the male nighthawk, Chordeiles
minor, incubating, this behavior is exceptional as nearly all of this duty
is performed by the female (Sutton and Spencer 1949). The female sits
on the two eggs steadily day and night except for short inattentive periods
of about 15 minutes soon after sunset in the evening and again in the
morning before sunrise (Collet 1934; Fiorucci 1941; Gilreath 1934; Gross,
see Bent 1940; Rust 1947). Collet once observed the male feed the incu-
bating female. The incubation period is 18 to 19 days long. After hatch-
ing, the young are brooded about 23 days and become largely independ-
ent after 30 or 34 days (Gross; Bowles 1921). They first begin to fly
short distances when 17 days old (Sutton and Spencer 1949). The
brooding is done mostly by the female, but the male may do so briefly
when he feeds the young. Both adults feed the young to varying pro-
portions in late evening and early morning (Bowles 1921, Pickwell and
Smith 1938, Wilson 1938).
Summary. The attentive behavior pattern in this family, which for
lack of further data, must be taken as representative of the order, includes
no nest building, usually crepuscular habits, nearly continuous incuba-
tion and brooding by the female except for short inattentive periods in
late evening and early morning, and joint responsibility of male and fe-
male for feeding the young. Nyctidromus is exceptional in the diurnal
changeover of the sexes on the nest and participation by the male more
extensively in incubation.
ORDER: APODIFORMES
There are two suborders here that need separate treatment, the swifts,
Apodi, and the hummingbirds, Trochili. Data are available on only one
of the two living families of swifts—the family Hemiprocnidae not being
included. There is only one family of hummingbirds, and it is limited
to the Western Hemisphere.
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EVOLUTION OF PARENTAL CARE 9921
Suborder: arovt; Family: apopipak. There is general agreement among
the various species studied in that both adults share about equally in
nest building, incubation, brooding, and feeding the young (Table 42).
In Apus apus it happens occasionally that only the female incubates (S. B.
Smith 1946). Nests are commonly made of sticks or other materials
fastened together with saliva. Even in Apus caffer, where use is made at
times of old swallow nests, the interior of the nest is covered with saliva.
Commonly a day elapses between laying of consecutive eggs. In the
black swift, Nephoecetes niger, there is record of the male feeding the
female on the nest (Michael 1927), and in Apus (Micropus) apus Koskim-
ies (1950) reports that the free adult may occasionally feed the incubat-
ing bird, but this behavior is not common in the family. Incubation is
very: irregular in the amount of time the adult birds spend on the eggs,
and there are frequent periods, sometimes two or six hours in dura-
tion, when neither bird is present. Either or both birds may incubate
at night when it is not uncommon to find both birds sitting side by side
on the nest sharing the duties of incubation. If only one bird is on the
eggs, the other bird will usually be roosting close by. In a personal com-
munication, Moreau mentions that this is a family in which there is
probably no parental care after the young leave the nest. Koskimies
verifies this for A. apus. Moreau also states that in African species atten-
tion to the young is as irregular as it is to the eggs. He points out that a
long period in the nest is inevitable when long flight feathers have to
be matured. In an all-day observation Bartels (1931) found that two
young Apus (Micropus) melba about three weeks old were fed at the
rate of 1.9 per hour. Bloesch (1931) reported observations at four nests
with two or three young each, varying from two days to four weeks of
age, where the average feeding rate was 0.7 per hour. Koskimies recorded
two young A. apus, three to four weeks old, fed during three days at an
average rate of 0.6 per hour but quotes observations of others of 1.0 per
hour and 1.5 per hour. Each feeding consisted of a mucous ball contain-
ing several hundred small insects which the adult accumulated in its
aerial flights. Lack (1951) gives the average rate of feeding in 25 broods
of A. apus over 920 hours as 1. 1 per hour. The rate of feeding the young
and the consequent length of time they spend in the nest vary directly
with weather conditions. Lack (1951) found the nestling period to vary
between 38 and 56 days in A. apus.
Suborder: Trocuitt; Family: TRocHitmae. In hummingbirds, the male
takes very little or no part in nesting after mating is consummated
(Table 42). Pitelka (1942) believes that recorded observations of the
male driving away intruders from near the nest is due to the chance
location of the nest in or near the male’s feeding territory. Moore (1947),
however, has collected the male of Colibri coruscans while incubating
999 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
eggs, and Cottam (1941) observed the male Stellula calliope feed the
incubating female by regurgitation on a number of occasions.
Nest construction may require a week (Skutch 1931), and additions
may be made after the eggs are laid. Normally there are two eggs, and
these are laid on alternate days (Aldrich 1945, Berlioz 1944, Clabaugh
1936, Skutch 1931). Incubation starts after the first egg is laid but may
not be fully established until the second egg appears. Hatching of the
second egg may occur twenty-four hours after the first (Berlioz 1944,
H. O. Wagner 1945). The incubation period is commonly 16 or 17 days —
and the nestling period 19 to 25 days (Skutch 1945d).
In Selasphorus sasin, Aldrich’s observations (1945) indicate the atten-
tive period during incubation averages 18.2 minutes and the inattentive
period, 4.3 minutes. Orr (1939) found the periods to average only 4.6
and 1.4 minutes, respectively, in the morning, but both he and Aldrich
agree that attentive periods become longer in the afternoon. DuBois
(1938) observed also in Selasphorus rufus that the female sat steadily
most of an afternoon except for an absence of one or two minutes in the
middle of the period. Skutch (Bent 1940) found in one female, Hylo-
charis leucotis, the average attentive period during the entire day to be
about 9.7 minutes and the inattentive period, 5.0 minutes. In four other
species, however, he found the attentive period more than an hour, the
longest attentive period of 99 minutes being in Phaeochroa cuvierii (per-
sonal communication). Bené (1940) found brooding in Archilochus
alexandri to continue for at least 10 days and attentive periods to aver-
age about 5.9 minutes. Skutch noted young Hylocharis leucotis brooded
until they were 17 to 18 days old. Orr (1939) states that brooding prac-
tically ceased when the young were 12 days old in Selasphorus sasin.
It appears that both young birds are fed by the female on each trip
to the nest (Common 1933, H. O. Wagner 1945). Nickell (1948) records
an unusual case of a female ruby-throated hummingbird, Archilochus
colubris, alternately feeding young at one nest and incubating eggs at
another nest. Additional feeding rates than those given in Table 42 are:
1.4 per hour for two young, 21 days old, in Topaza pella (E. M. Nichol-
son 1931); 2.6 per hour in Archilochus alexandri (Bené 1940, 1945) and
1.3 per hour (Common 1933) and 1.6 per hour in Archilochus colubris.
The latter figure is an average from four nests studied by students of
Dr. O. S. Pettingill, Jr., at the Michigan Biological Station.
Summary. There is agreement between the two suborders in that two
eggs are the usual number in a set and that the eggs are laid on alter-
nate days. In most other respects the behavior pattern for the two groups
differs widely. In the Apodi, both sexes share almost equally in all phases
of nest life; in the Trochili, the female does it all alone. In spite of that
the incubation and nestling periods are shorter in Trochili, and the atten-
EVOLUTION OF PARENTAL CARE 923
tive and inattentive rhythm is faster during incubation as is also the
feeding rate. .
ORDER: TROGONIFORMES
There is only one family in this order, and it is of tropical and sub-
tropical distribution. Skutch (1942, 1944c, 1948a) has made the only
worth-while nesting observations on this group.
Family: TROGONIDAE. Nests are usually excavated in the rotten wood
of a decaying trunk or stub; Trogon citreolus and sometimes T. massena,
however, make their burrow in a termite nest in a tree. T. caligatus oc-
cupies a wasp’s nest. There is no nest lining deposited. Both sexes share
nest building, incubation, brooding, and care of the young (Table 42).
The female is in the nest at night during the incubation period. The male
took a single long attentive period during the day in T. citreolus, T. curu-
cui, and at one nest of T. mexicanus. At another nest of T. mexicanus, the
male was on for three short periods during the day and the female for
the alternate periods and at night. In Pharomachrus, the male had a long
morning and a shorter afternoon attentive period; the female was in the
nest overnight and again for about four hours in late morning and early
afternoon. The attentive periods of both birds are sometimes interrupted
by absences of several minutes. It almost seems that in this species, and
perhaps also in T. mexicanus, that the behavior pattern is in the process
of changing to a more accelerated rhythm of shorter more numerous at-
tentive periods with more frequent alternation of the two sexes.
ORDER: CORACIIFORMES
This order includes many tropical and subtropical families. There are
four suborders, and fortunately there are nesting data for representative
species: in each. The only families not here included are the Todidae,
Leptosomatidae, and Phoeniculidae.
Suborder: aAucepINEs; Superfamily: ALCEDINOWEA; Family: ALCEDINIDAE.
These birds commonly nest in burrows dug in the side of banks. Some
tropical kingfishers nest in old swallow nests, in tree holes, or holes exca-
vated in insect nests in trees (Moreau, personal communication ). Both
sexes share nearly equally in all duties of nesting (Table 42). Skutch
(1933a) records that in Chloroceryle amazona and C. americana, the fe-
males incubate at night while the males do the major share of the incu-
bation during the day. In Ceryle torquata the routine was very different.
The two sexes alternated in the burrow once a day at 0700 or 0800
hours, so each bird incubated for a complete 24-hour period, with the
exception of a brief period during the afternoon when the eggs were left
uncovered. This behavior has not been reported, however, in Ceryle
alcyon, although there are no very detailed observations available for
IIA PARENTAL CARE AND ITS EVOLUTION IN BIRDS
as
the incubation period. Riviere (1933), R. L. Brown (1934), and Clancey
(1935) state that both sexes share in incubation and feeding the young
in Alcedo alcedo. The incubation period was found to be 19 to 21 days
and the nestling period usually 22 to 26 days. Although both sexes par-
ticipated in nest building, the male did the greater share of the digging.
Brown observed the male to be very energetic in feeding his sitting mate,
especially for a period after incubation commenced and again when the
young were newly hatched. Riviere found after the first day that the
average rate of feeding the young throughout the nestling period was
3.8 per hour. As the young grew, the size of the fish given them became
greater, and there was consequently no increase in the rate of feeding.
The attentive behavior pattern followed by Dacelo novaeguineae (gigas)
appears typical of the family as far as observations have been made
(Hindwood 1947).
Superfamily: MomMotoweEA; Family: MoMotTiIpAE. The only data avail-
able on the life history of birds in this family are two studies by Skutch
(1945e, 1947c; Table 42). Apparently both sexes participate in all phases
of the nesting duties. In Eumomota the female did the major share of
excavating the earthen nest burrow, but the male occasionally gave her
something to eat. In Aspatha underground burrows are used as sleeping
quarters throughout the year. Even while eggs and young are present,
both adults spend the night together. In Eumomota, however, only one
bird was observed on the eggs at night, and the burrow may be used
only during the nesting season.
Suborder: MERopES; Family: MEROPIDAE. Witherby et al. (1938) state
that in the bee eater, Merops apiaster, both sexes dig the nesting tunnel
and incubate the eggs. Koenig (1951) gives further details (Table 51).
Suborder: coracu; Family: cornacupar. The same authors record incu-
bation in the roller, Coracias garrulus, as 18 to 19 days and the nestling
period as 26 to 28 days. Incubation and care of young are shared by the
male and female. Nests are commonly in holes in old timber, mud banks,
crevices.
Family: upupmar. Nesting behavior in the hoopoe, Upupa epops
( Witherby et al. 1938, Skead 1950), differs from the above families in that
incubation is performed by the female alone. The female may be inatten-
tive for 30 minutes in early morning and late afternoon but is ordinarily
well supplied with food by the male. In three instances the male fed the
female three, five, and eight times per hour. Nests are located in tree
holes or other crevices. Four to eight eggs are laid, one daily, and the fe-
male begins staying in the nest when the first egg is laid. The incubation
period is uncertain, but data accumulated at two nests by Skead would
make it between 12 and 15 days. In the same article Hinde gives it as
16 days. The nestling period varies from 26 to 32 days. When the young
EVOLUTION OF PARENTAL CARE 995
hatch, the male brings food to the brooding female who then feeds the
young. This continues for seven to eight days, after which both male and
female feed the young directly. Four young were fed by three adults at
an average rate of 22 times per hour, but this rate appears unnaturally
high. Bussmann (1934) recorded a feeding rate for two young, 14 to
23 days of age, of only 1.9 times per hour.
Family: PHOENICULIDAE. In the wood-hoopoe, Rhinopomastus cyano-
melas, Hoesch (1933a) observed nesting behavior after the young
hatched. For the first day or so the female continued to stay in the nest,
and the male brought food for her and the young; thereafter both adults
sought food and brought it to the young about three times per hour.
Suborder: BUCEROTES; Family: BUCEROTIDAE. The hornbills are unique
in that the female, with the male’s help, plasters up most of the entrance
of her nest hole after entering, and remains throughout the period of
egg-laying, incubation, and at least part of the young’s developmental
period (Table 42). The total length of this time varies from six to eight
weeks in Tockus (Lophoceros) deckeni to as long as four months in
Bycanistes brevis. During all this time the female and her young are fed
by the male through a small opening in the plastered wall. In the genus
Tockus the female undergoes a sudden and complete molt while con-
fined in the nest, but this is not generally true of the family as a whole
(Moreau and Moreau 1940). The incubation period is probably about
40 days long in B. brevis and 28 to 36 days in various species of Tockus.
The females of Tockus, unlike Bycanistes, break out of their nest 2 to 4
weeks before the young are ready to leave and aid the male in bringing
food to the young until they are fully grown. Although the male Bycanis-
tes trips to the nest are not frequent, he commonly regurgitates as many
as 25 items of fruit on a single trip. Tockus males, on the other hand, are
more insectivorous and bring only a morsel at a time. North (1942) ob-
served the male Tockus (Lophoceros) erythrorhynchus feeding its mate
at the rate of 30 to 40 times per hour. This may be the reason why the
females of this genus leave the nest sooner and assist in the searching
of food for the young. Hoesch (1933) noted in Tockus (Lophoceros)
flavirostris that the male supplied the female and two young with food
for the first several days after hatching. Later the female left the nest to
feed the young almost alone at the rate of twice per hour, with the male
taking part only occasionally in the evenings. Furthermore, a brood of
Bycanistes may consist of only one or two young birds, while the brood
size in various species of Tockus varies from two to six (Moreau 1937,
Moreau and Moreau 1941).
Summary. The basic behavior pattern in this order is for both the
male and female to share more or less equally in nest building, incuba-
tion, brooding, and feeding the young. The attentive behavior pattern in
996 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
the Upupidae and the Bucerotidae has evolved at a tangent, and in the
Bucerotidae this tangent has become developed to an extreme. In a wide
variety of families, including the Upupidae, belonging to different orders,
the male often brings food to the incubating female who does all the
incubation. In the Bucerotidae, however, the male brings all her food, and
she is confined to the nest for periods of one and a half to four months.
Along with this confinement has developed the special behavior of
plastering shut all but a narrow crevice of the entrance hole, complete
molting of feathers in the female while in the nest cavity in at least cer-
tain species, the male exclusively feeding the female and the young dur-
ing the early part of their nest life, and other modifications of normal
behavior.
ORDER: PICIFORMES
There are two suborders. The suborder, Galbulae, is further sub-
divided into three superfamilies containing five families. The suborder,
Pici, however, contains but the one family.
Suborder: GALBULAE; Superfamily: GALBULOmEA; Family: GALBULIDAE.
Skutch (1937a) has the only available information on this family
(Table 43). In the black-chinned jacamar he found the female taking
the lead in excavating the kingfisher-like nest burrow in the ground,
but the male later assumed nearly equal share of the duties. They
worked for long periods, and the male fed the female at frequent inter-
vals. Both sexes shared incubation, brooding, and feeding the young on
nearly equal terms, except that the female was the one on the nest at
night. Since the two sexes alternated on the nest during the day, the
female secured most of her own food.
Family: BuccoN AE. Observations are available at only one nest of a
puffbird, that of Notharchus pectoralis (Skutch 1948c, Table 43). Both
sexes excavated the nest cavity in a tree at a leisurely rate, although one
sex was more active than the other. The three eggs are laid at intervals
of 2 days. Both sexes share incubation duties; the attentive periods are
irregular in length, varying from 7 to 162 minutes; and during the seven
hours of observation the eggs were covered only 70 per cent of the time.
Superfamily: CAPITONOIDEA; Family: caprroniDaE. In the prong-billed
barbet, Semnornis frantzii, Skutch (1944b) found both sexes participating
in nest building, incubation, and feeding the young (Table 43). This
is the only study of attentive behavior that has been found for this group.
Moreau (personal communication) states that there is a tendency for
some African barbets to approach the habits of Melanerpes (pp. 227, 231).
Family: tnptcatoripaE. The trait of parasitism has developed in this
small tropical family of honey guides, in at least Indicator indicator and
I. minor (Groebbels 1937).
EVOLUTION OF PARENTAL CARE 997
Superfamily: RAMPHASTOIDEA; Family: RAMPHASTIDAE. In addition to
studies on toucans made by Van Tyne (1929) and Skutch (1944a), given
in Table 43, H. O. Wagner (1944) has a little information on Aulacorhyn-
chus prasinus. In both genera, Aulacorhynchus and Ramphastos, the
sexes share the duties of incubation, brooding, and feeding the young,
although Wagner did not observe the male feeding the young. When
brooding two newly hatched young, Wagner states that “at each such
visit it remained inside some 20 or 30 minutes, which is about the same
length of time that it stayed away from the nest looking for food.” Skutch
found only one parent in the nest at night during incubation and through
most of the nestling period. In two subspecies of aracaris, Pteroglossus
torquatus, however, male and female may sleep in the nest cavity be-
fore the eggs are laid; during incubation a single parent attends the eggs
at night; but after the nestlings hatch, both parents sleep with them. The
long nestling period compared with the incubation period is worth not-
ing for this family.
Suborder: pict; Family: prciwaE. Both sexes participate in the excavat-
ing of the nest, although to a variable extent. In Melanerpes (Centurus)
carolinus, the red-bellied woodpecker, S. V. Wharram (personal com-
munication) watched nest building for 16 days and found that the birds
worked about 15 minutes at a period. Schuster (1936b) found Dendro-
copus (Dryobates) minor working in periods of 30 minutes, and Stein-
fatt (1940) observed the male D. medius working in periods of 9 to 23
minutes. Skutch (1948) recorded Melanerpes chrysauchen excavating
the burrow in 30-minute periods. In Dendrocopos (Dryobates) major
(Pynnodmen 1939), D. medius (Steinfatt 1940a), D. minor (Schuster
1936, Labitte 1945), D. martius (Niethammer 1938), D. pubescens
(Thoms 1927), Sphyrapicus thyroideus (Michael 1935), Picus canus
(Bussmann 1944), P. viridis (Steinfatt 1944a), and Melanerpes rubrica-
pillus (Centurus subelegans) (Skutch 1943) the male does most of this
work. Eygenraam (1947) reports that nest building in Dryocopus martius
lasts almost a month. At first both sexes share equally in the task, but
later the male works alone. Niethammer (1938) states that in Picus
viridis 14 days are required to excavate the nest cavity.
Both sexes take turns during the daytime in incubating the eggs. The
attentive periods commonly vary from one and a half to two and a half
hours in length; in Melanerpes chrysauchen and in Dendrocopos major,
the periods average only 23 minutes (Table 43). D. major may some-
times adhere to the time rhythm of other Picidae as Tracy (1938) found
the adults changing places about every two hours. In C. principalis Tan-
ner (1942) found the female relieving the male on the eggs between
0535 and 0730 hours in the morning and the male retiring in the evening
between 1530 and 1745 hours. This allows an active day of only about
228 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
10 hours. During the day the female incubated 6.5 hours and the male
3.5 hours, the sexes relieving each other on the eggs eight times. Accord-
ing to Eygenraam (1947), the female D. martius takes only three atten-
tive periods per day, 1.5 to 3.0 hours each. Likewise in Picus canus the
female is attentive only in the morning and in the afternoon, the male
is on the eggs during the middle of the day and at night (Bussmann
1944). The male D. medius is more attentive to incubation than the
female (Steinfatt 1940a).
There is nearly unanimous agreement, and Skutch (1933b) has dis-
cussed the fact, that the male incubates at night. One exception is that
Bussmann (1941) and Steinfatt (1941b) found the female Jynx torquilla
on at night. In Melanerpes chrysauchen, M. cruentatus, M. pucherani,
Picumnus olivaceus, and Picumnus aurifrons (lafresnayei), both the male
and female spend the night on the nest. In these cases it is probably the
male that actually sits on the eggs. The general rule in other orders is
for the female to incubate at night. Since in woodpeckers the male and
female both sleep in cavities throughout the year, and since the male
is usually the more energetic in making fresh cavities, Skutch (1943) sug-
gests that his cavity is the one the female selects for the nest and he
simply keeps on using it at night. Observations of Sherman (1910) on
Colaptes auratus support this contention in that male and female roosted
in separate but similar boxes before egg-laying but nested in the box
that the male had used.
The incubation period in many woodpeckers is short, 11 to 14 days.
It is longer in large species, as the pileated, Ceophloeus pileatus (18
days—Hoyt) and ivory-billed, Campephilus principalis. Likewise in the
genus Picus, Niethammer (1938) gives it as 15-17 days in viridis and
Bussmann (1944) gives it as 18 days in canus. The usually short in-
cubation period contrasts with a long period for the young to remain
in the nest, 19 to 35 days. Both adults share in the feeding of the
young, but the male is often more active in this duty than the female.
In addition to the data in Table 48, the following rates of feeding
have been recorded: Dendrocopos (Dryobates) minor—21.0 per hour
(Pynnonen 1939), 5.3 per hour (Steinfatt 1939d), 8.0 per hour
(Haverschmidt 1938); D. medius—5.0-13.7 per hour (Steinfatt 1940);
D. major—9.0 per hour (Haverschmidt 1938 ), 24 per hour (Tracy 1933),
6.0 per hour (Ris 1936); D. leucotus—6 per hour (Franz 1937), 2.0 per
hour (Pynnénen 1939); D. pubescens—29.8 per hour (Thoms 1927);
Picoides arcticus—9.6 per hour (England 1940); Picus viridis and P.
canus—1+ per hour (Bussmann 1933, 1944, Steinfatt 1944a); and Sphy-
rapicus varius—10.9 per hour (R. A. Johnson 1947), 15.9 (Shirling 1927).
Owen (1925) found D. major feeding young 20 times per hour with °
occasional inattentive periods of 30 minutes. Gebhardt (1940) recorded
EVOLUTION OF PARENTAL CARE 999
an exceptional case in Dryocopus martius when only the female fed the
young, in which she averaged 0.6 times per hour over 16 days of nest
life.
Leach (1925) and Ritter (1938) have described the very unusual
communal behavior of Melanerpes (Balanosphyra) formicivora. These
birds occur in small flocks throughout the year, and several birds may
roost together in the same cavity. Only one bird, however, stays on the
eggs at night. Three, four, or five birds of both sexes may work in
relays at excavating the nest hole, incubating, and feeding the young.
If this is not true communal breeding, then it may be that a nesting
pair is simply being assisted by unmated, possibly immature, birds of
both sexes. The behavior of Picumnus lafresnayei may represent a stage
of evolution toward communal behavior not quite so far advanced as in
M. formicivora. Skutch (1948b) describes how one male and two fe-
males roosted in the nest hole that contained two eggs. During the day
the male and at least one female took turns at incubation.
Summary. In this order the male usually takes a preponderant part
in nest building, incubation, brooding, and feeding the young. At least
in the Picidae he also does most of the incubating and brooding at night.
The basic pattern is an alternation of male and female in all the nesting
duties, and it is probable that the evolutionary trend toward a greater
male load is from an older, more equal division of duties. The reason for
believing this is that in Galbula, the genus lowest in the taxonomic series,
the female takes the lead in nest building, incubates at night, and the
two sexes share nearly equally in incubating the eggs during the day,
while in Dendrocopos, and possibly Dryocopus, which are near the top
of the taxonomic series, the relation is reversed. Eygenraam (1947) states
that in Dryocopus martius the female takes the leading role in courtship
which is in harmony with the reversed role of the sexes.
Dendrocopos represents an advanced development of the behavior
pattern in other ways. This genus has the short nesting period of 34 days
from the time the eggs are laid until the young fly. The incubation period
is only 12 days and is correlated with short attentive periods. The genus
has some of the most rapid feeding rates in the entire order. In general,
the behavior pattern approaches that of the next and highest order, the
Passeriformes. It should be noted, however, not only in this genus but
also in the Picidae and Ramphastidae, in general, that short incubation
periods are joined with long periods for the young to stay in the nest.
ORDER: PASSERIFORMES
This is the largest order of birds and the most highly advanced and
specialized. Four suborders are recognized. There are no data available
on the suborder, Eurylaimi, with its single family of broadbills. In the
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EVOLUTION OF PARENTAL CARE 933
suborder, Tyranni, there are two superfamilies. Information is not avail-
able on seven of the thirteen families. There are data on one of the two
families of the suborder, Menurae. In the large suborder of songbirds,
Passeres, there is no breakdown into superfamilies, and this group is
represented by data on 34 families. Fifteen families are not included.
Some families have been divided into subfamilies, but these are indi-
cated only in the Fringillidae where there are enough data available to
permit some reliable estimation of their significance in the analysis of
behavior patterns.
Suborder: TYRANNI, Superfamily: FURNARIOWEA; Family: DENDROCOLAP-
TiDAE. Skutch’s (1945a) observations on the nesting behavior of the allied
woodhewer (Table 44) show that both adults participate in nest build-
ing, incubation, brooding, and feeding the young. For a time after hatch-
ing, brooding is nearly continuous, but as the young mature, it decreases
in amount during the day but continues at night until the young are 12
days old. In the wedge-billed woodhewer, Glyphorhynchus cuneatus,
both sexes also alternate at incubation, but in the Carriker dendrocincla,
Dendrocincla anabatina, no more than one bird has been seen partici-
pating in any phase of nest life.
Family: FurNarmpAE. Alexander F. Skutch has kindly supplied me with
unpublished data on the attentive behavior of this family. Much of this
material is summarized in Table 44. Apparently both sexes participate in
nest building. This was also observed in Furnarius leucopus and Cranio-
leuca erythrops.
Both sexes commonly share incubation, brooding, and feeding the
young, although at one nest of P. boissonneautii only the female was ob-
served to do so. Eighteen hours observation were taken during the incu-
bation period of A. ochrolaemus. The six attentive periods ranged from
62 to over 138 minutes in duration. Five attentive periods were measured
during six hours observation of P. boissonneautii, and these varied from
3 to 93 minutes. During ten hours with S. brachyura the male had nine
attentive periods ranging from 4 to 44 minutes, and the female had eight
periods ranging from 18 to 44 minutes. During five hours spent with S.
erythrothorax, the three attentive periods of the male ranged from 14 to
18 minutes and the six periods of the female ranged from 6 to 40 min-
utes. Nine hours were spent with X. minutus where the nine attentive
periods varied from 12 to 118 minutes. Finally, in S. quatemalensis four
attentive periods during six hours ranged from 54 to 74 minutes in length.
Skutch states that the nestling period in this family commonly ranges
from 13 to 29 days. In addition to the species listed in Table 44, he found
two feathered nestlings of Rhopoctitis rufo-brunneus to be fed 11 times
in four hours or at the rate of 2.8 times per hour. The rates of feeding
234 PARENTAL CARE AND ITS EVOLUTION IN BIRDS
given in Table 44 are based on only three or four hours observation in
each case.
Family: FormMicartupAE. Skutch (1945b) writes: “Antbirds as a rule
take long sessions on the eggs, male and female replacing each other in-
frequently. Even the smaller species often sit for two or three hours
without interruption; and once I watched an antpitta (Grallaria perspi-
cillata) incubate for five hours without a break. At least in those species
in which the sexes can be distinguished, the male usually takes some-
what longer sessions on the eggs by day than the female; but the female
sits through the night.”
Gross (1927) recorded that in the spotted antbird, Hylophylax naevio-
ides, and spotted-crowned ant-vireo, Dysithamnus puncticeps, the two
sexes alternate at incubation duties and in the latter species the attentive
periods likewise are long, being two or three hours throughout the day.
In 90 hours observation at nine nests of nine different species, each
with two young between 1 and 9 days of age, Skutch (1949a) found
the rate of feeding by the two parents to be 1.3 to 5.3 times per hour.
He (1945d) records incubation periods for various species between 14
and 17 days and nestling periods between 9 and 13 days. It is unusual
to have nestling periods so much shorter than incubation periods. Data
for four species are compiled in Table 44.
Superfamily: TyRANNOWEA; Family: coTincmar. The few observations
on Platypsaris aglaiae and Tityra semifasciata, mostly made by Skutch
(Table 44), indicate that the male sometimes aids the female in nest
building and regularly feeds the young, but only the female incubates the
eggs and broods the young. He (1945) gives an incubation period of 18
to 19 days for Pachyramphus polychopterus and in three other species
indicates that the nestling period is at least 19 days long. In a personal
communication he indicates that the nestling period may extend to 25
days in this family.
Family: prertDaE. Skutch (1949c) has the only study of attentiveness
in this family (Table 44). An interval of 3 or more days occurs between
the laying of the two eggs. This slow reproductive rate is further shown
by the long incubation period, the long attentive and inattentive periods,
and the very low feeding rate. In a personal communication he gives the
incubation period as 19 to 21 days for this family and the nestling period,
13 to 15 days.
Family: TyRANNIDAE. Bent (1942) has summarized the data for North
American flycatchers and some detailed data are presented in Table 44.
From 3 to 10 days are used in nest building. The female does most of
this work (see also Tinkham 1949), but the male occasionally aids in some
species. All recent studies indicate that the female is solely responsible
for incubation of the eggs, yet in the earlier literature there is frequent
EVOLUTION OF PARENTAL CARE 935
reference to the male sharing these duties in several species. Further at-
tention should be directed to this point. The male has been observed
feeding the female in Sayornis saya, Empidonax wrighti, and Contopus
cinereus, in addition to those listed in Table 44. The incubation period
varies rather widely between the various genera of this family from 18-
19 days in the tropical Megarhynchus to 12-13 days in Contopus and
Tyrannus.
Normally only the female broods the young after hatching, but both
sexes feed the young in many species. Skutch writes me that the male
apparently takes no part in nesting in Myiobius, Pipromorpha, Rhyn-
chocyclus, Oncostoma, Onychorhynchus, and Terenotriccus, except that
in Onychorhynchus he guards the nest. The male may occasionally stand
on the nest rim and shade the young from the sun in T. tyrannus and E.
minimus. This family is remarkable in the fast rates at which the young
are fed. In addition to those listed, Saunders (1938) recorded a rate of
24 feedings per hour of two young in E. minimus and Lawrence (1948a )
found the same rate at another nest; Bent (1942) gives 24 feedings per
hour for E. difficilis, 30 feedings per hour in E. traillii, and 14 feedings per
hour in Myiarchus cinerascens. Fitch (1950), however, found three to
four young Muscivora forficata fed only 1.7 times per hour by the male
and 5.1 times per hour by the female. Since all these species are fly-
catchers in habit as well as in name, probably the amount of food they
bring to the young on each visit is small, hence the large number of trips
they usually need to take. Lawrence (1948) observed the adults bring-
ing only one fly per trip during the first four days, but later four to five
flies per trip.
Megarhynchus has a very slow rhythm for the entire nesting cycle, in-
cluding a 2- or 3-day interval between laying of successive eggs. In
writing about the black-tailed myiobius, Myiobius atricaudus, Gross
(1927) states:
As is the case with many birds in the Tropics, this flycatcher frequently left
the eggs for long periods of time during the warmer hours of the day, but she
always faithfully brooded them at night. So far as I could determine only one
bird, probably the female, did the work concerned in rearing the brood . . .
the incubation period of eggs was 21 days, whereas the flycatchers in the tem-
perate regions hatch in much less time. .. . Further the time spent by the young
of this species in the nest was three weeks... .
Suborder: MENURAE; Family: MENURIDAE. Tregellas (1931) states that
only the female lyrebird, Menura sp., is concerned with nest building,
incubation, and raising of young. This is verified by Ward (1939). About
a month is required to build the nest and the one egg is not laid for
another week or two. Incubation begins after still another week.
Ward (1940) found that 28 days were required to hatch a fresh egg under
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