Chapter I: Part 1

UNIVERSITY OF KANSAS PUBLICATIONS
MUSEUM OF NATURAL HISTORY

Volume 12, No. 5, pp. 241-296, 6 figs.
March 7, 1962

Natural History of the Bell Vireo,
Vireo bellii Audubon

BY
JON C. BARLOW

UNIVERSITY OF KANSAS
LAWRENCE
1962

UNIVERSITY OF KANSAS PUBLICATIONS, MUSEUM OF NATURAL HISTORY

Editors: E. Raymond Hall, Chairman, Theodore H. Eaton, Jr.,
Henry S. Fitch

Volume 12, No. 5, pp. 241-296, 6 figs.
Published March 7, 1962

UNIVERSITY OF KANSAS
Lawrence, Kansas

PRINTED BY
JEAN M. NEIBARGER, STATE PRINTER
TOPEKA, KANSAS
1962

29-1506

Natural History of the Bell Vireo, Vireo bellii Audubon

BY

JON C. BARLOW

CONTENTS

PAGE
CONTENTS 243
INTRODUCTION 245
ACKNOWLEDGMENTS 245
METHODS OF STUDY 246
STUDY AREA 247
Considerations of Habitat 248
SEASONAL MOVEMENT 250
Arrival in Spring 250
Fall Departure 251
GENERAL BEHAVIOR 252
Flight 252
Foraging and Food Habits 252
Bathing 253
VOCALIZATIONS 254
Singing Postures 255
Flight Song 255
Daily Frequency of Song 255
Types of Vocalizations 255
TERRITORIALITY 258
Establishment of Territory 259
Size of Territories 259
Permanence of Territories 260
Maintenance of Territory 260
Aggressive Behavior of the Female 264
Interspecific Relationships 264
Discussion 265
COURTSHIP BEHAVIOR 267
Displays and Postures 268
Discussion 270
SELECTION OF NEST-SITE AND NESTBUILDING 272
Building 274
Gathering of Nesting Materials 276
Length and Hours of Nestbuilding 277
Abortive Nestbuilding Efforts 277
Renesting 277
The Nest 277
EGGLAYING AND INCUBATION 278
Egglaying 278
Clutch-size 279
Incubation 280
The Roles of the Sexes in Incubation 280
Relief of Partners in Incubation 283
NESTLING PERIOD 283
Hatching Sequence 283
Development of the Nestlings 284
Parental Behavior 285
Feeding of the Nestlings 286
Nest Sanitation 287
Fledging 287
Nest Parasites 287
FLEDGLING LIFE 288
Second Broods 288
REPRODUCTIVE SUCCESS 289
Behavior 290
Predation 291
Cowbird Parasitism 291
SUMMARY 292
LITERATURE CITED 294

INTRODUCTION

The Bell Vireo (_Vireo bellii_ Aud.) is a summer resident in riparian and second growth situations in the central United States south of North Dakota. In the last two decades this bird has become fairly common in western, and to a lesser extent in central, Indiana and is apparently shifting its breeding range eastward in that state (Mumford, 1952; Nolan, 1960). In northeastern Kansas the species breeds commonly and occurs in most tracts of suitable habitat.

The literature contains several reports dealing exclusively with the Bell Vireo, notably those of Bennett (1917), Nice (1929), Du Bois (1940), Pitelka and Koestner (1942), Hensley (1950) and Mumford (1952). Bent (1950) has summarized the information available on the species through 1943. Nolan (1960) recently completed an extensive report based on a small, banded population at Bloomington, Monroe County, Indiana. He validated for this species many points of natural history previously based on estimates and approximations, especially concerning the post-fledging life of the young and the movement of the adults from one "home range" to another in the course of a single season.

None of these reports, however, has emphasized the ritualized behavioral patterns associated with the maintenance of territory and with courtship. Among the North American Vireonidae, the behavior of the Red-eyed Vireo (_Vireo olivaceus_) is best documented (Sutton, 1949; Lawrence, 1953; Southern, 1958). With this species authors have concentrated on the mechanics of the breeding season and their reports contain little discussion of the aggressive and epigamic behavior of the bird.

The amount of information on the ritualized behavior of the Bell Vireo and related species heretofore has been meager. I observed breeding behavior from its inception in early May through the summer of 1960. It is hoped the resulting information will serve as a basis of comparison in future studies of behavior of vireos; such ethological data are becoming increasingly important, especially as an aid in systematics.

ACKNOWLEDGMENTS

To professors Frank B. Cross, Henry S. Fitch, and Richard F. Johnston of the Department of Zoology of the University of Kansas I am grateful for comments and suggestions in various phases of the study and the preparation of the manuscript. Professor Johnston also made available data on the breeding of the Bell Vireo from the files of the Kansas Ornithological Society. I am indebted to my wife, Judith Barlow, for many hours of typing and copy reading. Mrs. Lorna Cordonnier prepared the map, Thomas H. Swearingen drew the histograms, and Professor A. B. Leonard photographed and developed the histograms. Dr. Robert M. Mengel contributed the sketch of the Bell Vireo and George P. Young prepared the dummy Bell Vireo used in the field work. Thomas R. Barlow, Donald A. Distler, Abbot S. Gaunt, John L. Lenz, Gary L. Packard, A. Wayne Wiens, and John Wellman assisted in various phases of the field work.

METHODS OF STUDY

Daily observations were made from May 11 to June 26 in 1959 and from April 15 through July 15 in 1960. Six additional visits were made to the study area in September of 1959, and ten others in July and August, 1960. Periods of from one hour to eleven hours were spent in the field each day, and a total of about five hundred hours were logged in the field.

Each territory was visited for at least five minutes each day but more often for twenty minutes. The breeding activities of the pairs were rarely synchronous. Consequently several stages in the cycle of building were simultaneously available for study.

Nine young and one adult were banded in 1959. No Bell Vireos were banded in 1960. Individual pairs could be recognized because of their exclusive use of certain segments of the study area and by the individual variation in the song of the males. Sexes were distinguishable on the basis of differences in vocalizations and plumages.

Most nests were located by the observer searching, watching a pair engaged in building, or following a singing male until the increased tempo of his song indicated proximity to a nest. As the season progressed and the foliage grew more dense, it became increasingly difficult to locate completed nests. Blinds were unnecessary because of the density of vegetation. Observations were facilitated by a 7 x 50 binocular. Data were recorded on the spot in a field notebook. Eggs were numbered by means of Higgins Engrossing ink as they were laid.

Individual trees in which males sang most were marked over a three-week period. Then the distances between the most remote perches were paced. These distances aided in determining the size of the territories. The general configuration of the vegetation within each territory determined the location of one or more boundaries of the territory. Each territory was given a number, 1, 2, 3, etc., as it was discovered; consequently there is no numerical relationship between the designations of the territories established in 1959 and 1960. Nests within a territory were designated as 1-a, 1-b, 1-c, etc.

Although experimentation was not a primary source of data, it proved useful in certain instances. A stuffed Blue Jay elicited mobbing behavior from nesting pairs. A dummy Bell Vireo elicited both agonistic and epigamic behavior from nesting pairs, depending on the phase of the nesting cycle.

The temperature at the beginning of each day's work was taken by means of a Weston dial thermometer. A hand counter and a pocket watch having a second hand were used in determining such data as frequency of song and periods of attentiveness by the sexes. Histological cross-sections, prepared by A. Wayne Wiens, of the ventral epidermis of both sexes were used to study brood patches.

STUDY AREA

The intensive field work was on a 39-acre tract (fig. 1) extending approximately 7/10 of a mile west from U. S. highway 59, which in 1959-1960 constituted the western city limit of Lawrence, Douglas County, Kansas. The eastern boundary of the study area is approximately 1-1/2 miles southwest of the County Courthouse in Lawrence. The eastern ten acres is associated with the Laboratory of Aquatic Biology of the University of Kansas. The 15 acres adjacent to this on the southwest is owned by the University of Kansas Endowment Association, but is used by Mr. E. H. Chamney for the grazing of cattle. This portion is bounded on the west by a stone fence, beyond which lies a 14-acre field of natural prairie owned by Dr. C. D. Clark that is bordered on the extreme west by a narrow thicket of elm saplings.

The principal topographic feature of the area is an arm of Mount Oread, that rises some 80 feet above the surrounding countryside. About 200 feet from the crest of the southwestern slope of the hill a 40-foot-wide diversion terrace directs run-off toward the two-acre reservoir that is the source of water for eight experimental fish ponds of the laboratory.

The predominant shrub-vegetation consists of Osage orange (_Maclura pomifera_), honey locust (_Gleditsia triacanthos_), and American elm (_Ulmus americana_). These saplings, ranging in height from 3 to 25 feet, grow in dense thickets as well as singly and in clumps of twos and threes. Larger trees of these same species grow along the crest of the hill, along the eastern and southeastern boundaries of the area, and along the stone fence separating University land from that owned by Dr. Clark. A dense growth of coralberry (_Symphoricarpos orbiculatus_) forms the understory just below the crest of the hill. Isolated clumps of dogwood (_Cornus drummondi_) and hawthorn (_Crataegus mollis_) are scattered throughout the area. These species of shrubs grow densely along the stone fence. The isolated thicket on the Clark land is composed primarily of elm and boxelder (_Acer negundo_), but includes scattered clumps of dogwood, Osage orange, and honey locust. Poplars (_Populus deltoides_) are the only large trees in this area.

The open areas between the thickets are grown up in red top (_Triodia flava_), bluestem (_Andropogon scoparius_), Switchgrass (_Panicum virgatum_), Kentucky bluegrass (_Poa pratensis_), bush clover (_Lespedeza capitata_) and mullen (_Verbascum thapsus_). Shrubby vegetation occupies about 65 per cent of the total area, but in the Clark portion constitutes only about 35 per cent of the ground cover.

_Considerations of Habitat_

Nolan (1960:226), summarizing the available information on habitat preferences of the Bell Vireo, indicates that this species tolerates "a rather wide range of differences in cover." He pointed out that a significant factor in habitat selection by this species may be avoidance of the White-eyed Vireo (_V. griseus_) where the two species are sympatric.

In Douglas County where the Bell Vireo is the common species, the White-eyed Vireo reaches the western extent of its known breeding range in Kansas. At the Natural History Reservation of the University of Kansas, where both species breed, the Bell Vireo occurs in "brush thickets in open places" (Fitch, 1958:270) and the White-eyed Vireo occupies "brush thickets, scrubby woodland and woodland edge" (Fitch, _op. cit._, 268). Along the Missouri River in extreme northeastern Kansas, Linsdale (1928:588-589) found the White-eyed Vireo "at the edge of the timber on the bluff, and in small clearings in the timber," while "the Bell Vireo was characteristic of the growths of willow thickets on newly formed sand bars." Elsewhere in northeastern Kansas I have found the Bell Vireo in shrubbery of varying density and often in habitat indistinguishable from that occupied by White-eyed Vireos at the Natural History Reservation. In the periphery of the region of sympatry the rarer species is confronted with a much higher population density of the common species and consequently might well be limited primarily to habitat less suitable for the common species. This would seem to be the case in eastern Kansas, presuming that interspecific competition exists.

The Bell Vireo has followed the prairie peninsula into Indiana, aided by the development of land for agriculture. In nearby Kentucky where thousands of miles of forest edge are found, and where little brushy habitat of the type preferred by the Bell Vireo occurs, the White-eyed Vireo is abundant whereas the Bell Vireo is unknown as a breeding bird (R. M. Mengel, personal communication).

In more central portions of the area of sympatry, nevertheless, the two species do occur within the same habitat (Ridgway, 1889:191; Bent, 1950:254) and occasionally within the same thicket (Ridgway, in Pitelka and Koestner, 1942:105); their morphological and behavioral differences, although slight, probably minimize interspecific conflict. The Bell Vireo and the Black-capped Vireo (_V. atricapillus_) have been found nesting in the same tree in Oklahoma by Bunker (1910:72); the nest of the black-cap was situated centrally and that of the Bell Vireo peripherally in the tree. Bell Vireos invariably place their nests in the outer portions of trees and peripherally in thickets. This placement would further obviate interspecific conflict with the white-eye since its nests are placed centrally in the denser portions of a thicket.

A critical feature of the habitat preferred by the Bell Vireo is the presence of water. In far western Kansas this species is restricted to riparian growth along the more permanent waterways. This in itself is not adequate proof of the significance of water supply because thicket growth in that part of the state is found only along waterways. The 20 areas over the state that I have visited where Bell Vireos were present were closely associated with at least a semi-permanent source of water. Fifteen other areas indistinguishable from the 20 just mentioned, but lacking a permanent supply of water, also lacked Bell Vireos. Nevertheless areas in which Bell Vireos typically nest are decidedly less mesic than those frequented by White-eyed Vireos.

Once the Bell Vireo was probably more local in its distribution being restricted to thickets associated with permanent water. Clearing of woodland for agricultural and other use, and subsequent encroachment of second growth concomitant with the creation of man-made lakes and ponds, has greatly increased the available habitat for this bird. The preferred species of shrubs for nesting are reported (Bent, 1950:254) to be various wild plums (_Prunus sp._). The widespread distribution and abundance of the exotic Osage orange has greatly augmented the supply of trees suitable for nesting.

SEASONAL MOVEMENT

_Arrival in Spring_

The subspecies of the Bell Vireo breeding in Kansas, _V. b. bellii_, winters regularly from Guerrero and the Isthmus of Tehuantepec south to Guatemala, El Salvador, and northern Nicaragua (A. O. U. Check-list, Fifth Edition, 1957:469-470). In the United States migrating birds are first recorded in early March (Cooke, 1909:119). The Bell Vireo is a relatively slow migrator, moving primarily at night and covering little more than 20 miles at a time (Cooke, _op. cit._ 119). The average date of arrival, based on 27 records, for northeastern Kansas is May 8; the earliest record is April 22, 1925, from Manhattan, Riley County, Kansas (fig. 2-A).

In 1959 the first bird arrived at the study tract about May 5. No additional birds were heard singing until the third week of the month, in which eight new males were noted. As mentioned, in 1960 field work was begun in mid-April and the study area was traversed daily. No birds were detected until late afternoon of May 3, when one, presumably a male, was seen foraging.

Lawrence (1953:50) has reported that males of the Red-eyed Vireo precede females in the breeding area by as much as two weeks; the male Red-eyed Vireo forages but sings little in the pre-nesting period. The male Bell Vireo arrives first at the breeding area but precedes the female by only a few days. On the morning of May 4 the first male was singing from a number of perches while ranging over an area of seven acres. This area encompassed territories later occupied by three pairs, 2 (1960), 4 (1960), and 5 (1960). Late on the afternoon of May 4 the first courtship songs were heard and the first male was seen with a mate at 6:20 p.m. Eight additional males arrived from May 6 through May 18. A tenth male was discovered in the vicinity of territory 9 (1960) on June 18, 1960.

_Fall Departure_

The average date of departure for 21 years in northeastern Kansas is September 3 (fig. 2-B). The earliest date is August 14 from Concordia, Cloud County, Kansas (Porter, unpublished field notes). The latest date is September 27 (Bent, 1950:262) from Onaga, Pottawatomie County, Kansas. In 1959 the last vireo was seen at the study tract on September 14. The birds do not all depart at the same time. On September 1 there were still five singing males in the study area; by September 10 there were three and on September 13, only one.

GENERAL BEHAVIOR

_Flight_

In "straight-away" flight the Bell Vireo undulates slightly. In a typical flight several rapid, but shallow, wing beats precede a fixed-wing glide of from 1 to 15 feet in length. Because the wings are extended horizontally during the glide, the bird does not move distinctly above or below the plane of flight. The White-eyed Vireo generally appears to be slower and more lethargic in flight than the Bell Vireo. In the breeding season most flights of the Bell Vireo are no longer than a few feet between adjacent shrubs and trees, but occasional sustained flights are as long as 300 feet. The birds fly as low as 2 feet above ground, but have often been observed as high as 70 feet above the ground.

In courtship and protracted territorial disputes, where chase between sexual partners or a pair of antagonists occurs, looping flights are observed. The wings are beaten as the birds climb and many aerial maneuvers are performed in the course of the glide.

_Foraging and Food Habits_

The Bell Vireo has been characterized as a thicket forager (Hamilton, 1958:311; Pitelka and Koestner, 1942:104), but in my experience it is not restricted to low level strata; birds forage from ground level upward, both in thickets and isolated trees ranging in height from 3 feet to 65 feet. The tendency to forage at higher levels is in part dictated by the presence of tall trees within the various territories.

Territories 1 through 7 (1960) contained from three to ten trees surpassing 40 feet in height. They grew singly or in small groves. The Bell Vireos foraged fully 20 per cent of the time in these trees. Food was sought throughout the leaf canopy.

Behavior in foraging in larger trees followed a routine pattern. Typically a pair alighted in a tree at a height of 15 feet. Then the female hopped to a perch a foot above the one upon which she landed. The male succeeded her to the perch she had previously occupied. The pair in effect spiraled around some large, essentially upright, branch, in foraging. The birds usually reached higher perches in this manner rather than by flying upward 10 to 15 feet to them. This manner of progression within a tree is reminiscent of a similar habit of the _Cyanocitta_ jays. Presumably, the habit of the Bell Vireo of foraging in higher strata is facilitated by the absence of other species of arboreal foraging vireos.

Chapin (1925:25) found the Bell Vireo to be more insectivorous in its food habits than any other North American vireo. He found 99.3 per cent of all food contained in 52 stomachs to be of animal origin. Only three times have I seen a Bell Vireo take food of vegetable origin. On September 9, 10, and 14, 1959, I noted a male eating wild cherries over a period of 65 minutes of observation. Chapin (1925:27) noted that beginning in July vegetable matter represented 1.57 per cent of the bird's subsistence, and thereafter slightly more until fall migration.

Animal food, consisting primarily of insects and spiders, is actively sought along branches and under leaves. Often a foraging bird will leap to the underside of a branch and hover, mothlike, beneath a cluster of leaves while extracting some insect. Some individuals hung upside down on small branches, paridlike, while foraging. Lawrence (1953:710), and Southern (1958:201) have recorded similar behavior of the Red-eyed Vireo. Occasionally, I have seen a Bell Vireo fly from a perch and capture an insect in the manner of a flycatcher. The birds do not appear to be adept at this type of food-getting. Nolan (1960:242) mentions Bell Vireos holding hard-bodied insects by means of their feet while breaking the exoskeleton with the beak to obtain the soft parts. Southern (1958:201) recorded a female Red-eyed Vireo foraging on the ground; I have seen a Bell Vireo on the ground but once, and it was gathering nesting material.

_Bathing_

On May 14, 1960, in a rill that empties into the northeastern edge of the reservoir a female flew down from a perch six inches above the surface, barely dipped into the water, flew to a perch 12 inches above the water, violently shook her ruffled body feathers, quivered her wings, and rapidly flicked her fanned tail. The entire procedure was repeated three times in five minutes. She was accompanied by a singing male that did not bathe.

Nolan (1960:241) reports a male Bell Vireo bathing by rubbing against leaves wet with dew; he notes that the White-eyed Vireo bathes in a similar manner. Southern (1958:201) twice observed Red-eyed Vireos bathing in water that dropped from wet leaves. In my study area in 1960, only territories 7, 8, 9, and 10 were not immediately adjacent to permanent water. The pairs of Bell Vireos in those territories presumably had to reply on wet vegetation for bathing.

VOCALIZATIONS

The male Bell Vireo begins to sing regularly soon after its arrival in spring. Some daily singing continues following the cessation of breeding activities until departure of the species in late summer or early fall. The highest sustained rate of song occurs on the first and second days of nest building. Because careful records of meteorological data were not kept, I cannot significantly correlate rates of song and specific temperatures and other weather conditions. Frequency of song was reduced when the temperature rose above 90 deg. F., as it did on many days in June, 1960. Nice (1929:17) mentions a similar decrease in singing when the temperature exceeded 85 deg. F.

Passerine birds typically sing at a high rate throughout courtship and nestbuilding, but at a markedly lower rate thereafter. Most vireos are atypical in this respect. In the study area in 1960 Bell Vireos sang more often than Robins, Mockingbirds, Field Sparrows, Brown Thrashers, Catbirds, and Doves breeding in the same habitat, about as often as the Meadow Larks in the adjacent fields, and less often than Painted Buntings.

The Bell Vireo seems to sing less often in the undisturbed state than when aware of the presence of an observer. Observations from my car, at a site approximately equidistant from territories 1 (1960), 2 (1960), 4 (1960), and 6 (1960) indicate that the rate of song during incubation is decidedly less when no disturbing influence is present. Normally, in this period, song aids in maintaining contact between the members of a pair, serving to locate the male as he forages. Mumford (1952:230) noted that the males often came out to meet him as he entered their territories, singing as they approached. The male typically continues to sing for some time after the intruder has departed. Here the song acquires the additional functions of alerting the female to danger and threatening the trespasser. Even after allowance is made for this reaction to disturbance, Bell Vireos sing more often than most of their nesting associates, and, on a seasonal basis, they are vocal for a much longer time.

_Singing Postures_

In the normal singing posture the body of the Bell Vireo is maintained at an angle of 35 deg. to the horizontal. Occasionally, during nest building, I have observed the body held at angles as severe as 80 deg. from the horizontal.

The head of the White-eyed Vireo is distinctly bobbed up and down, two or three times, during the utterance of a song phrase. A bob involves a deliberate withdrawal of the head towards the body and subsequent sharp, almost vertical, extension of the neck. The head of the Bell Vireo does not bob, although it vibrates as the song is delivered.

_Flight Song_

The Bell Vireo does not have a distinctive flight song; in fact, it rarely sings or calls while in flight. Nolan (1960:240) has recorded a male singing the normal song while in flight. Sharp scold-notes are uttered in mid-air when a bird is agitated or actually attacking an enemy. These notes and songs recorded by Nolan hardly qualify as flight song, for this term implies use of a distinctive vocalization not uttered in other circumstances.

_Daily Frequency of Song_

In the morning, Bell Vireos usually began singing a few minutes before sunrise. Their songs were invariably preceded in the study area by those of Western Kingbirds, Robins, Mourning Doves, Mockingbirds, Cardinals and Meadow Larks. Bell Vireos sang relatively little after 6:30 p.m., even on the longest days of the year. The latest daytime singing that was recorded was seven songs at 7:18 p.m. on June 20, 1960. A Cardinal in the vicinity sang for a full hour after this.

_Types of Vocalizations_

Six vocalizations were readily distinguishable in the field. These are divisible into songs and call notes.

1. Primary song. It has been described by Pitelka and Koestner (1942:103) as an "irregular series of harsh and sharp, but slurred notes preceded by a few distinct notes of the same quality and ending with a decided ascending or descending note of similar harshness." The terminal note may also be somewhat abbreviated and intermediate between an ascending or descending note. The song is sometimes delivered as a couplet that consists of a phrase ending on a descending note. This delivery is typical of incubation and later renesting. During early season activities, the bird utters a phrase ending on the descending note as many as 15 times before a phrase ending on an ascending note is heard.

A sonagram of a single phrase, one of several recorded on May 9, 1960 (the third day of building of nest 1-b 1960), consists of 10 notes, the first of which is distinct. The remaining notes are slurred. This phrase is 1.4 seconds in length.

Songs are delivered most rapidly in the course of territorial disputes and defense. The song is loudest in times of nestbuilding and periods of aggressive behavior. At these times, on clear, calm days, the songs are audible 100 yards away. Singing in the nestling period and post-breeding season is audible at distances of no more than 50 feet; such notes have been termed "whisper songs." Table 1 summarizes singing rates at different periods of the nesting cycle in several situations and under various weather conditions.

Songs are of equal frequency in the immediate vicinity of the nest and elsewhere in the territory. Nice (1929:17) also found this to be true. Perches can be almost at ground level or as high as 60 feet. Forty per cent of my data on song concern singing at heights of more than 20 feet. As indicated in foraging, the lack of competition from aboreal species of vireos presumably contributes to the use of higher perches by Bell Vireos.

No female song was recorded in 1959, but on May 26, 1960, a female was heard to sing once. She appeared at nest 1-f (1960) shortly after the male arrived. Unlike him, she did not participate in building, but seemed to be inspecting the nest. After 30 seconds she sang once--a low garbled phrase--and also scolded once. After this she left. In the meantime the continuously singing male moved two feet away from the nest, then back to it and resumed construction.

The song of the female signaled to the male her departure. Pitelka and Koestner (1942:103) heard a female sing twice after she replaced the male on the nest. Females of three other species of vireos, the Black-capped Vireo, _V. atricapillus_ (Lloyd, 1887:295), the Philadelphia Vireo, _V. philadelphicus_ (Lewis, 1921:33), and the Latimer Vireo, _V. latimeri_ (Spaulding _in_ Pitelka and Koestner, 1942:103) have been heard singing. Lewis and Spaulding also suggest that the song of the female functions as a signal prior to exchange at the nest.

The primary song identifies the singer as a male Bell Vireo. It aids in securing a mate and in warning potential adversaries; also, the song is a signal in certain situations and serves to locate the male.

TABLE 1. REPRESENTATIVE SINGING RATES OF BREEDING BELL VIREOS.
ALL RATES WERE AT AIR TEMPERATURES LESS THAN 86 deg. F. EACH
INSTANCE REPRESENTS APPROXIMATELY 30 MINUTES OF OBSERVATION.

====================================================================
| | Average
Circumstance | Instances | rate per
| | minute
----------------------------------------------+-----------+---------
Attraction of mate | 2 | 6.3
Territorial dispute | 5 | 12.8
Nestbuilding | 6 | 7.0
Egglaying | 1 | 3.0
Incubation | 6 | 3.9
Exchange of partners in the incubation period | 1 | 4.0[A]
Foraging | 2 | 2.2
"Morning" song | 1 | 28.6[A]
"Evening" song | 1 | 1.9[A]
----------------------------------------------+-----------+---------
Over-all average rate per minute 6.3

[A] Not sustained; data representative of periods less than 5
minutes in length.

2. Courtship song. It is here termed the "congested" song and is comparable to the adult "run-on" song mentioned by Nolan (1960:240). The congested song is a squeaky version of the primary song and is given when birds are engaged in pair-formation, nestbuilding, and egglaying. The delivery is rapid and the sound can be likened to that made by rapidly scraping a bow across a taut violin string. Nolan (_in_ Mumford, 1952:230) is probably speaking of this song when he describes a "tuneless" song that "had a jerky, sputtering quality that characterizes part of the song of the Ruby-crowned Kinglet (_Regulus calendula_)." More recently (1960:240) he applies the adjectives "twanging," "Bobolink-like," "bubbling," "jerky," and "squeaky." This song is often blended with the primary song and is audible for 75 feet.

A specialized version of the congested song is associated with pre-and post-copulatory display but differs from the typical squeaky performance in terminating in two ascending notes reminiscent of the ascending phrase of the primary song.

3. Distress call. It was heard only once, when a captured bird was being freed from a net. When the bird was almost disentangled it uttered 10 high-pitched, plaintive notes. The quality of the notes suggested a relationship to the song phrase rather than to other types of vocalization. A nesting pair of Bell Vireos, 10 feet away, became extremely excited when they heard the distress notes. They "scolded" vigorously and flew around my head at a distance of six feet.

4. Alarm note. This is a specialized, three-note call of the male and was heard only from the onset of pair-formation through early nestbuilding. This whinnying, flickerlike call, phonetically _eh-eH-EH_, each succeeding note of which is louder than the one before, is given whenever the male is disturbed by an unfamiliar object. This call is generally succeeded by the _chee_, but occasionally blends into an extended "whinny," and is typically given from some perch affording an unobstructed view of the offending object. The male stretches his neck and cocks his head, the wings and tail are not flicked or fanned, and no feather tracts are erected. The bird, nevertheless, flits nervously from perch to perch when uttering the call.

5. The _zip_. The male has a special "scold" note of his own that is heard when an intruder first approaches the nest. Phonetically it is _zip-zip-zip_. It is not so loud as the _chee_, and the delivery is more deliberate than that note. If the intruder remains near the nest, the _zip_ is usually replaced by the _chee_.

6. The generalized call note or _chee_. The call notes associated with several situations are combined under this subheading since all can be rendered in English by the same phonetic equivalent--_chee_. The _chee_ associated with nestbuilding is of moderate pitch and delivered deliberately at a rate of about 40 per minute. The feeding call of the adults is a soft slurred _chee_, while that of the nestlings has a mewing quality. In general, the _chee_ utilized in signal situations consists of a few repetitions of the basic note emitted at a moderate pitch. The _chee_ associated with hostile and courtship behavior is higher pitched and the delivery is much more rapid, approximately 200 per minute. Nolan (1960:240) reports a continuous rate of 25 per five seconds when an adult Bell Vireo is alarmed. The _chee_ of extreme anxiety is a loud emphatic buzz, phonetically ZZ-ZZ-ZZ-ZZ.

TERRITORIALITY

The Bell Vireo exhibits "classic" passerine territoriality. Within a specific area, a pair of this species carries out pair-formation, courtship activities, copulation, nesting, rearing the young, and foraging. With the cessation of reproductive activities, a pair continues to restrict its other daily activities to the same general area.

_Establishment of Territory_

In early May the segment of the total suitable habitat within which a Bell Vireo restricts its activities is not rigidly defined and the first male of the season ranges over an area too large to be maintained permanently--one that seems greatly to exceed the needs of breeding. Male 1 (1960), for instance, was first seen foraging over an area of approximately seven acres. With the influx of other males, portions of this large tract were usurped and the territory of the original male was gradually reduced to an area of little more than an acre.

In this initial period, a male becomes identified with a large area but is restricted to an area of nearly typical size by the encroachment of other males. Territorial disputes in this period often involve physical contact, as well as protracted sessions of high-intensity singing at rates exceeding three hundred song-phrases per hour.

Eventually the carrying capacity of the habitat is reached and no further partitioning occurs. The beginning of nestbuilding coincides with this relative stabilization of the territorial boundaries. Through the remainder of the cycle of behavior associated with any one nest, all activity is that of the occupant pair within its territory.

_Size of Territories_

The nine original territories established in 1960 varied in size from 0.26 acre to 3.1 acres (Table 2). Fitch (1958:270) found the territories of several pairs of Bell Vireos at the University of Kansas Natural History Reservation to vary from 0.4 to 1 acre. Hensley (1950:243) estimated the size of the territory of a pair of Bell Vireos observed in Piatt County, Illinois, at 3.1 acres. Nolan (1960:227) records home ranges of 2 to 3 acres. The pairs that he studied were sole occupants of fields several acres larger than the portions actually utilized. His description of the vegetation indicates that most of the second growth was not much taller than 7 feet. As indicated elsewhere, the second-growth in my tract averaged 15 feet tall. The smaller average size of territory (1.25 acres) that I found is probably a function both of this greater vertical range of available foraging area and the much higher gross density of birds (40 pairs per 100 acres).

_Permanence of Territories_

Most pairs remain in their original territories throughout the summer, although some shift certain territorial boundaries. In 1960 pairs 2 and 6, in the course of selecting a site for a replacement nest, annexed adjacent areas previously occupied by other pairs. Pair 2 relocated in a space that originally included territories 1 and 4, and pair 6 built a nest in an area formerly occupied by pair 7. Males 1 and 4 were sacrificed for specimens and pair 7 probably was destroyed by a predator. Owing to the presence of a nest, the annexed area becomes the focal point of the activities of a pair, but the original area is regularly visited and may be returned to in a later renesting.

TABLE 2. SIZE OF THE NINE ORIGINAL TERRITORIES OCCUPIED IN 1960.

==========================================
| Date first |
Territory | occupied | Dimensions
-------------+--------------+-------------
1. | May 3, 1960 | 1.6 acres
2. | May 5, 1960 | 0.6 acre
3. | May 7, 1960 | 0.26 acre
4. | May 11, 1960 | 1.03 acres
5. | May 12, 1960 | 2.07 acres
6. | May 14, 1960 | 3.1 acres
7. | May 13, 1960 | 1.7 acres
8. | May 14, 1960 | 0.46 acre
9. | May 14, 1960 | 0.4 acre
-------------+--------------+-------------
Average 1.25 acres

_Maintenance of Territory_

Except in the early stages of nesting, territory is maintained primarily by song. In the period of incubation a male regularly patrols his territory between sessions of sitting on the eggs. He sings several songs from each of several perches. A male follows a predictable path, rarely traveling more than 150 feet from the nest. Incipient patrolling is seen early in the breeding season when territorial boundaries are in a state of flux.

The male White-eyed Vireo travels a semi-predictable route, as does the Solitary Vireo (R. F. Johnston, MS). According to Lawrence (1953:50), the male Red-eyed Vireo has a distinct singing area completely divorced from the nest area dominated by the female. Southern (1958:109), working with this same species in Michigan, did not recognize separate areas, but found that the male wandered randomly over the territory.

In a species so highly active as the Bell Vireo, the degrees of hostile action associated with an encounter overlap in such a fashion that no clearcut distinction can be drawn among the various displays. Nevertheless, certain generalized patterns are characteristic of all situations in which members of this species are in a state of anxiety. The threat displays described in the succeeding paragraphs may all be utilized within as little as two minutes; mutual agonism may be terminated at any stage by concerted attack of the dominant bird.

1. Vocal threat. When an intruder is discovered the resident male markedly increases his rate of singing. The alarm note, _eh-eH-EH_, is the first call uttered during the nestbuilding and egglaying periods.

2. Head-forward threat. If the intruder does not flee, the resident male adopts a specific threat posture. The head and neck are extended. The feathers of the crown are erected, but those of the body are sleeked. The bird crouches slightly and the tail is flicked laterally, but not fanned. The intensity of the singing increases and is supplemented by scolding, also delivered at a rapid rate. The intruder normally retreats at this juncture.

3. Wing-flicking and submaximal tail-fanning. If the interloper remains, the anxiety of the resident male increases. He slightly depresses the tail and, at the same time, rapidly fans and closes it. The tail is only partially fanned. The wings are held slightly away from the body and rapidly flicked above the back. This flicking should not be confused with quivering of the wings associated with begging and other solicitory postures. Song is now almost completely replaced by high-intensity scolding. Associated with this high degree of anxiety are displacement behaviorisms, including bill-wiping, reversal of direction on a single perch, and a nervous hopping from one perch to another.

4. Ruffling and maximum tail-fanning. This display is most often seen in conjunction with the harassment of predators, but occasionally it is observed in territorial disputes occurring at the boundary of adjacent territories where neither male is strictly dominant and in which there is much vacillation prior to attack. The feathers of the abdomen are ruffled. The term "ruffled" pertains to a full erection of the feathers, giving a ragged appearance to the body outline (Morris, 1956:80). Ruffling of the abdominal feathers emphasizes their yellow color and seemingly heightens the intimidatory effect. The tail is fully fanned, and so maintained, for a few seconds at a time; it is held at a 45 deg. angle to the body. The scold becomes an extremely intense, stacatto buzz, ZZ-ZZ-ZZ-ZZ.

5. Supplanting attack. The attack directed against a trespassing male is initiated as a lunge that results in a collision with the opponent in mid-air or on his perch. The bird attacked is struck by his adversary's open beak or body.

Hinde (1952:71-72) indicates four courses of action followed by a Great Tit (_Parus major_) when attacked under similar circumstances. "(a) It flies away: The attacker usually flies after it and a chase ensues. (b) It shifts its perch a few inches: the attacker lands in its place, and both usually show head-up postures. (c) It remains where it is, but adopts a head-up posture: the attacker usually then shows upright flight. (d) It may fly up and meet the attacker in mid-air: in that case an actual combat may result, or both combatants may show upright flight."

Head-up posturing and upright flight are not presently recognized components of the behavior of the Bell Vireo. The behavior of the attacked Bell Vireo is similar to that described in (a), (b), and (d) above, and is clearly dictated by the proximity of his own "home base."

Eleven disputes among occupants of adjacent territories were witnessed between May 6 and June 3, 1960, in which some or all of the described threat displays were manifest (Table 3). In each instance, patrolling males were gradually attracted to each other. As they approached, their rates of song increased from an average of six repetitions per minute to 15 per minute. Eight of the disputes involved physical combat.

On May 6, 1960, when male 2 (1960) was in the process of usurping an eastern segment of the original territory of male 1 (1960), a violent, protracted dispute was observed. By this date male 1 (1960) had obtained a mate and had begun construction of nest 1-a (1960); male 2 (1960) had not yet acquired a mate. At first the two males were singing vigorously, from one to 10 feet apart. Female 1 (1960) followed her mate closely and scolded, at the same time partially fanning her tail. In the course of vocal dueling the males had traveled to within 50 feet of nest 1-a (1960), when male 1 (1960) suddenly lunged at 2 (1960). The males plunged to the ground, locking bills and clutching at each other with their feet as they fell. As soon as they touched the ground they separated. Male 2 flew east with male 1 in pursuit. This conflict lasted three minutes.

Additional physical combat was witnessed several minutes later. This again involved striking with the bill, wings and feet. A high pitched squeaky _chee_ was uttered by both combatants. The female scolded from a nearby perch. Upon separating, the males engaged in a wild, looping flight. At about 350 feet from nest 1-a (1960), the chase abruptly ended. For ten minutes thereafter, both males sang at a high rate from perches about 10 feet apart. This terminated the physical combat, but three additional protracted, vocal duels occurred in the remainder of the morning.

TABLE 3. INTRASPECIFIC DISPUTES IN MAINTENANCE OF TERRITORY.

Behavior

==============================================================
| Number | | | Average
| of | Vocal | | length of
| conflicts | dueling | Combat | disputes
-------------+-----------+---------+--------+-----------------
Prenesting | 3 | 3 | 2 | 6 min. 40 sec.
Building | 8 | 8 | 6 | 3 min. 8 sec.
Incubation | 1[B] | 1 | ... | 20 min.
+-----------+---------+--------+-----------------
Totals | 12 | 12 | 8 | 5 min. 30 sec.
-------------+-----------+---------+--------+-----------------

[B] Directed against a stuffed Bell Vireo.

Probably as a direct result of these conflicts, a neutral zone approximately 300 feet wide developed between the two territories. By May 14 this intervening area was occupied by male 4 (1960). By this date both 1 (1960) and 2 (1960) were involved in nestbuilding and 4 (1960) was not challenged for several days.

Maximum tail-fanning prior to attack also appears as an element of aggressive behavior in White-eyed Vireos. A brief skirmish between a male of this species and a small, greenish passerine was observed at the Natural History Reservation on May 25, 1960. The White-eyed Vireo was singing from a perch 30 feet high in a dead elm, when the unidentified passerine landed 10 feet distant. The white-eye ceased regular song and uttered several catbirdlike calls, and at the same time slightly depressed and fully fanned the tail. After 10 seconds, the white-eye lunged at the intruder, striking it in mid-air. A brief looping flight ensued through the branches of the elm before the intruder was able effectively to retreat.

_Aggressive Behavior of the Female_

The female Bell Vireo is concerned primarily with the defense of the nest and the young and she rarely assists the male in defense of distant parts of the territory. She employs the same threat displays as the male.

_Interspecific Relationships_

A number of meetings between Bell Vireos and other species were observed in the course of the study (Table 4). Resident pairs of this species exhibited different degrees of tolerance toward other species. Many birds, including Cardinals, Field Sparrows, Painted Buntings and Mourning Doves were ignored completely. Chickadees evoked responses characterized by slight increase in song and some anxiety; this was perhaps owing to similarity in size, motion and call notes. Warblers, when met with, were invariably chased. They may be momentarily mistaken for rival vireos.

TABLE 4. INTERSPECIFIC CONFLICT OBSERVED IN 1959 AND 1960.

==================================================================
| Number | Phase of | Behavior of
| | | Bell Vireos
Species | of | breeding +------+---+----+---
|conflicts| cycle |HFT[C]| S | TF | A
---------------------+---------+--------------+------+---+----+---
_Coccyzus | 1 | Nestling | | | |
americanus_ | | period | -- | x | |
| | | | | |
_Cyanocitta | 3[D] | Nestling and | | | |
cristata_ | | incubation | | | |
| | period | x | x | x | x
| | | | | |
_Parus atricapillus_ | 1 | Prenesting | -- | x | |
| | | | | |
_Molothrus ater_ | 1 | Nestling | | | |
| | period | -- | x | -- | x
| | | | | |
_Dendroica petechia_ | 1 | Prenesting | -- | x | -- | x
| | | | | |
_Geothlypis trichas_ | 1 | Nestbuilding | -- | x | -- | x
| | | | | |
_Pituophis | | | | | |
catenifer_[E] | 1 | Post-fledging| -- | x | -- | x
---------------------+---------+--------------+------+---+----+---

[C] HFT = head-forward threat; S = scolding;
TF = tail-fanning; A = attack.

[D] Includes attack against a dummy Blue Jay.

[E] The Bull Snake is here included because the vireos
directed typical aggressive displays towards it.

Blue Jays were vigorously attacked, especially late in incubation and throughout the nestling period of the Bell Vireo. I did not see a jay struck, but a vireo would circle one closely as it perched and pursue it when it flew, following as far as 100 yards beyond territorial bounds. The buzz, ZZ-ZZ-ZZ-ZZ, was uttered in conjunction with this harassment.

A stuffed jay placed eight feet from a nest elicited threat display and displacement behavior from the owners of the nest, but no attack. Incubation had just begun at this nest. A dummy Bell Vireo placed close to another nest only momentarily disturbed the male, and the female completely ignored it. Incubation had also recently begun at this nest. At this same general stage, moreover, nesting pairs showed little inclination to harass me.

_Discussion_

Hinde (1956:341-342) indicates that territory has been defined in a number of ways by many workers. All of the definitions involve modification of Howard's classic "defended area." Pitelka (1959:253) has reacted against this behaviorally-oriented concept. He thinks that the concept of territory should be based on exclusive use of an area by its occupants, and not so much the defense by which they maintain it.

Methods of treating territoriality in the Bell Vireo seemingly incorporate features of both schools of thought. The area used exclusively for all biological needs by a single pair of Bell Vireos is vigorously defended both physically and vocally early in the breeding season and vocally as the season progresses.

In the period of territorial establishment a relatively large area is actively defended. The building of a nest establishes a focal point of activity in a somewhat more restricted area than that originally occupied. After the success or failure of a nest, a new site is selected to which the focal point of activity is shifted. If suitable habitat adjacent to the extant territory is unoccupied by other Bell Vireos the unoccupied area may be annexed in the course of searching for a new site. Such annexation occurs only when pairs formerly occupying adjacent suitable habitat disappear from this territory; possibly the size of the territory of any one pair is dictated by the density of population of the species as well as by the presence of suitable habitat. This may not always be true as indicated by Kliujver (1951:40), who in studying the Great Tit, found no appreciable difference in the size of territory in two different habitats even though there was a marked difference in population density of the birds.

Fluctuation of territorial boundaries is not uncommon in passerines, especially when no rivals exist to contest movement. Hinde (1956:351) indicates that fluctuations in size of territory are to be expected although the territories of different species of birds have different mean sizes.

Once nesting activities commence there is a marked reduction in the amount of territory utilized and a distinct decrease in the aggressive tendencies of the male; it would seem that energy previously utilized in regular fighting is rechanneled for nestbuilding, incubation and care of the young. Further, contraction of the area of activity obviates high-intensity territorial defense, as adjacent males, even in regions of high population density, are isolated from one another by an area no longer regularly traversed.

With cessation of breeding activities physiological mechanisms governing maintenance of territory seemingly are no longer active and yet the pairs of Bell Vireos remain within a restricted area which they alone use. Earlier definitions of territory as a "defended area" do not adequately cover such situations and yet from the standpoint of Pitelka the area still retains the characteristics of true territory. In fact, territory as defined by Pitelka is clearly manifest at this time. Whether the birds remain in an area through "force of habit" is of little consequence.

I have retained the term "territory" in preference to the term "home range" used by Nolan (1960:227). His failure to observe territorial defense is responsible for his terminology, although it is readily understandable that such defense would be lacking in a population of relatively low density in which pairs were isolated from one another by areas of unfavorable habitat. This isolation in itself would tend to preclude territorial conflict but territories were, in fact, maintained.

The marked similarity in the essential features of aggressive behavior in North American vireos attests to their close relationship. Flicking and fanning of the tail are distinct components of the hostile behavior of the Bell Vireo, White-eyed Vireo, Red-eyed Vireo (Lawrence, 1953:69), and the Black-whiskered Vireo (_Vireo altiloquus_; Bent, 1950:319), and, presumably, of the remaining species of the genus. The occurrence of these same displays as intrinsic behavioral elements of interspecific hostility suggests a common derivation. Moynihan (1955:256) indicates that all intraspecific hostile displays, and probably most interspecific hostile displays, evolved originally as social signals having the same general function. Further, Hinde (1956:344) points out that there is a fundamental similarity in the motor patterns used in fighting in different contexts, including both interspecific and intraspecific fighting.

COURTSHIP BEHAVIOR

The precise mechanism of pair-formation in the Bell Vireo is not known. My experience has been to find a male one day and then one or two days later to discover that it has a mate. Lawrence (1953:53), tells of a male Red-eyed Vireo singling out a female from a flock of migrants passing through his territory and violently driving her to the ground. Shortly after this attack the pair was seen searching for a nest site. But such an incident has not been reported for other vireos, nor have I witnessed such behavior myself.

Early courtship activities of the Bell Vireo are characteristically violent affairs, with the male directing strong aggressive attacks toward the female. Rapid, looping flights through the thickets occur, the female leading the male. Occasionally he deliberately collides with her in mid-air, but the pair quickly separate. This violent sexual chasing is manifest prior to the inception of nestbuilding. With commencement of this activity, sexual chases through the territory subside.

Absence of sexual dimorphism in the Bell Vireo obviously suggests that behavioral criteria are used by the birds in sex-recognition. The lack of aggression by the female upon initial aggression by the male is an essential component of recognition of sex; she is clearly subordinate. Such subordination is also the significant feature of continued sex-recognition. Courtship display by a resident male, directed toward a stuffed male and a wounded male which sat motionless, supports the contention that a subordinate or submissive attitude of the female is a key factor in sex-determination.

Nestbuilding and courtship are intimately associated in this species. The male constructs the suspension apparatus of the nest, the completion of which coincides with the assumption of nestbuilding activity by the female. Roles of the sexes in nestbuilding are described in the section on nestbuilding. The male frequently interrupts construction to court the female. This, in combination with perpetual song as he works, serves to strengthen the pair-bond and stimulate nestbuilding tendencies of the female.

It is doubtful that any attempts at copulation are successful up to this time. The female is singularly unresponsive to the advances of the male; a female retreats before most violent attacks and is seemingly oblivious to less vigorous behavior. After the female assumes the responsibility of building, the tempo of courtship activities increases.