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.
The female becomes increasingly more receptive and her work is often
interrupted by advances of the male. Copulation occurs frequently from
about the third day of nestbuilding through the first day of
egglaying, a period of four to six days. Male displays and
vocalizations associated with courtship continue through the fourth or
fifth day of incubation.
_Displays and Postures_
The principal courtship displays and postures that were seen
throughout the nestbuilding phase are as follows:
1. Greeting ceremonies. Both birds are crouched from one to five
inches apart. The feathers on one (the male?) are sleeked, and on the
other are fluffed. Fluffing (Morris, 1956:80) denotes partial erection
of the body feathers producing a rounded, unbroken body line and is
not to be confused with ruffling, mentioned in the sections pertaining
to territoriality and pre- and post-copulatory display. Fluffing is
generally considered to be an appeasement display and it is seen in a
variety of situations involving a dominant-subordinate relationship.
Both birds flick wings and tails rapidly and reverse directions on
their perches frequently. A low, rapid _chee_ is uttered during this
performance. This ceremony is repeated often in the first three days
of nestbuilding, but less frequently thereafter. It usually occurs
after building by one or both partners and prior to another trip in
search of nesting material. It lasts from 10 to 50 seconds and is not
immediately followed by any additional courtship activities. Nolan
(1960:228-229) observed mutual displays between periods of violent
sexual chase that suggest that the greeting ceremonies that I have
described are an integral part of pair-formation as well as a
component of continued maintenance of the bond.
2. "Pouncing." The female rapidly quarter-fans and partially depresses
her tail. She utters a high pitched scold (_chee_). The male, from a
perch within two feet of the female, fans the tail fully and depresses
it vertically, and, with mouth open, lunges at the female; or, with
similar tail mannerisms, the abdominal feathers ruffled, the wings
held horizontally, and the primaries spread, he sways from side to
side from four to six times, and then lunges at the female. The male
is silent when he pounces; the _chee_ or the courtship song is emitted
when swaying precedes pouncing. The male strikes the female with his
breast or with his open beak. The female rarely flees although she is
usually displaced several inches along the branch upon which she is
sitting. However, the female may fly several inches to a new perch.
The failure of the female to adopt a solicitation posture presumably
indicates sexual unreadiness. Instances of the male deliberately
colliding with the female as she flies in the course of gathering
nesting material are probably analogous to pouncing. In none of the
above situations are females observed to fight back in any way. Nice
(1943:174) believed pouncing to be analogous to sexual chasing found
in such species as the Red-winged Blackbird. In the Song Sparrow,
pouncing is observed most often in the first and second days of
nestbuilding.
3. "Leap-flutter." The male, in the course of displaying with the tail
fanned before the female, suddenly leaps eight inches to ten inches
vertically and flutters in mid-air several seconds, before dropping to
the original perch. This display occurs in full view of the female. It
is often associated with pouncing and is also seen prior to
copulation. In the latter instance it is probably pragmatically
functional, for it permits the male to orient above the female before
dropping to her back to copulate. No vocalization is uttered during
the leap-flutter.
4. Pre-copulatory display (Fig. 3). The male faces the female. The
tail is fanned fully and depressed at a sharp vertical angle to the
body. Body feathers, both dorsal and ventral, are ruffled, almost
tripling the apparent volume of the thorax. The head is withdrawn and
slightly thrown back. Feathers of the head are not erected. The mouth
is opened wide. The legs are slightly flexed and the body is swayed
laterally. Horizontally, the head and body traverse an arc of about
100 deg.; vertically, they traverse an arc slightly less than 180 deg.. At the
low point of any one swing, the delivery of the courtship song begins.
At the termination of the swing the two normal, ascending notes are
emitted. This performance may last as long as three minutes.
[Illustration: FIG. 3. A single male Bell Vireo in the
pre-copulatory display. Note the ruffled dorsal and ventral
body feathers. The male on the left has reached the zenith of
a single swing. The male on the right has nearly reached the
low point of a swing.]
The pre-copulatory display of the male elicits receptive behavior in
the female. She crouches in a solicitous manner, with the body
feathers fluffed and the tail raised slightly, and utters a muted
_chee_.
5. Copulation. The male abruptly terminates his swaying display with a
leap-flutter that positions him above the female's back. He then
descends and copulation occurs. The male continues to flutter his
wings to maintain balance throughout the two seconds of cloacal
contact. Following an unsuccessful copulation on June 23, 1960,
displacement preening and bill wiping were performed by both sexes.
6. Post-copulatory display. On June 25, 1960, after a second attempt
at copulation with a stuffed bird in which semen was actually
deposited on the dummy's back, male 10 (1960) performed a swaying
display. In this instance, however, instead of addressing the dummy
from the front, the male alighted one inch to the right of the stuffed
bird. When swaying to the left (toward the dummy) the head of the
displaying male actually passed above the neck of the stuffed bird.
This ritualized behavior could conceivably be derived from
hetero-preening.
_Discussion_
Within the scope of my research it was difficult to detect the
over-all sequence of epigamic displays that result in synchronization
of the physiological states of the sexes throughout the period of
courtship. Possibly all displays, except the post-copulatory one,
occur in no particular order in the courtship period. However, each
ritualized display seemingly strengthens the pair-bond.
Swaying has been recorded in a variety of situations of a sexual and
semi-sexual nature for the Solitary Vireo (_V. solitarius_; Townsend,
1920:158) and the Red-eyed Vireo (Tyler, 1912:230; Bent, 1950:342). In
every instance the body feathers of the swaying birds were sleeked.
Courtship behavior in any species of North American vireo seems
closely to resemble that of any other; pairing and nestbuilding of a
female _V. solitarius_ and a male _V. flavifrons_ as reported by
Hauser (1959:383) support the idea of close resemblance.
A marked similarity will be detected between certain basic elements of
aggressive and epigamic displays. These basic elements are wing- and
tail-flicking, tail-fanning, and high-intensity delivery of the
_chee_. Pouncing and supplanting attacks are essentially similar. Such
similarities suggest either a common origin for certain aggressive and
epigamic displays or the derivation of one from the other.
High-intensity _cheeing_ is obviously a function of excitement,
whether in conjunction with hostility or sexual behavior. According to
Andrew (1956:179), flicking of wing and tail in passerines are
intention movements of flight. These actions have been emancipated
from incomplete take-offs and incorporated in ritualized courtship and
agonistic behavior. In incipient courtship behavior the male is
governed by three conflicting tendencies; to flee, to attack, or to
behave sexually before his mate (Tinbergen and Hinde, 1958:256). When
pairing, Bell Vireos interrupt sexual chase with "greeting
ceremonies," the male's tendency to attack and the female's tendency
to flee are momentarily reduced, and the forming bond is strengthened.
Thus, the intention movements become an integral part of courtship.
In situations where attacking and fleeing are the two conflicting
tendencies, wing-flicking and tail-flicking are incorporated into
threat display, but do not lose all of their original function, for
they facilitate attack. Tail-fanning, as a display element, increases
the awesome aspect of the threatening bird and in courtship presumably
makes the sexes more attractive to one another.
Courtship feeding has not been recorded for the Bell Vireo. In
general, it is unknown in North American vireos, with the exception of
the red-eye (Lawrence, 1953:53). It would serve no "practical" purpose
in the Bell Vireo since the male regularly relieves the female during
incubation, thus allowing her ample opportunity to forage. In the
Red-eyed Vireo, only the female regularly incubates, and courtship
feeding is definitely functional. Nolan (1960:228) described a brief
pecking or pulling with their bills between pairing birds. This may be
incipient "symbolic" courtship feeding, or perhaps mutual preening.
SELECTION OF NEST-SITE AND NESTBUILDING
As far as can be determined, the nest-site is selected by the female.
Typically, the pair makes short, low-level flights from tree to tree
with the female invariably in the lead. The birds usually forage
within each tree; the female interrupts this activity to inspect small
forks of low, pendant branches and the male occasionally pauses to
sing. The singing is loud but not particularly regular, as it is later
when the male accompanies the female during actual nestbuilding.
Method of selection of site resembles that described by Lawrence
(1953:53) for the Red-eyed Vireo.
Nests are suspended from lateral or terminal forks about 27 inches
high in bushes and small trees that, in the study area, averaged 11
feet, four inches in height (Table 5). The height above ground of the
nests does not vary appreciably as the season progresses as is the
case with nests of Red-eyed Vireos, for which Lawrence (1953:54) noted
that late nests were placed higher than those built earlier in the
season.
Most nests are so situated that they are protected and concealed by
the dense foliage of trees. Where nests are placed in low bushes, as
coralberry or dogwood, the bush is invariably overhung by the foliage
of a much taller shrub or tree.
The nest tree or shrub was in every instance situated at the edge of a
thicket or isolated from adjacent trees by several feet. Preference
for open situations is characteristic of the species. In contrast, the
nest of the White-eyed Vireo (Bent, 1950:229) is placed toward the
center of thickets.
In the choice of sites in the study area, the Bell Vireos were almost
unopposed by other avian species, owing to the size of the fork
utilized and the fact that the nests are located peripherally, rather
than centrally, in the bush or tree. This lack of competition for a
nest-site provides a Bell Vireo with an ample supply of nest-sites
within any one territory.
TABLE 5. NEST-SITES UTILIZED IN 1960.
====================================================================
| Number | Average | Average
Plant | of | height of | height of
| nests | plant | nest
-----------------------------+--------+---------------+-------------
_Ulmus americana_ | 4 | 7 ft. 6 in. | 2 ft. 3 in.
_Maclura pomifera_ | 20 | 13 ft. 11 in. | 1 ft. 11 in.
_Crataegus mollis_ | 1 | 11 ft. | 3 ft. 1 in.
_Gleditsia triacanthos_ | 2 | 15 ft. 6 in. | 1 ft. 9 in.
_Acer negundo_ | 4 | 8 ft. 9 in. | 2 ft. 5 in.
_Cornus drummondi_ | 2 | 8 ft. | 2 ft. 8 in.
_Symphoricarpos orbiculatus_ | 3 | 3 ft. | 1 ft. 10 in.
| | |
7 | 36 | 11 ft. 4 in. | 2 ft. 3 in.
-----------------------------+--------+---------------+-------------
Selection of the first nest-site may take as long as two days,
possibly owing to incomplete development of the nesting tendency, but
more likely to a general lack of familiarity with the territory.
Red-eyed Vireos require five to six days to choose the first nest-site
(Lawrence, 1953:54). Later sites of the Bell Vireo are chosen in as
little as three hours. Nest 1-c (1960) was abandoned at about 11:00
a.m. on May 14, 1960, when part of the thicket on the edge of which
this nest was located was removed by brush-cutters clearing a power
line right-of-way. By 2:00 p.m. this pair had begun construction of
1-d (1960) in an Osage orange 110 feet southwest of 1-c (1960).
This particular site is of further interest because it is the same one
utilized for nest 1-a (1960). In all, four instances of utilization of
a nest-site a second time were recorded. Two-a (1960) and 2-d (1960)
were built in the same fork; 1-c (1960) and 1-h (1960) were in the
same tree, but not the same fork. It should be mentioned that 1-a
(1960) and 2-a (1960) were abortive attempts that did not progress
beyond the suspension apparatus. Nice (1929:16) recorded a similar
instance of the re-use of a nest tree, but different forks were used.
Re-use of an exact nest-site would ordinarily be impossible if the
initial attempt were not abortive, because the presence of a completed
nest would pose problems in construction with which the birds would
probably be unable to cope. (A report by Morse in Bent, 1950:256 of a
double nest indicates that this may not always be true. At the time of
discovery one nest contained two eggs and the other nest contained
young.) Since nests are used only once there would be no tendency to
adopt the old nest. However, abortive nests, usually little more than
a few strands of nesting material secured to the fork, might stimulate
the birds to continue building. Re-use of a single nest-site in 15.8
per cent of 38 nests built in 1960 seems to be more than fortuitous
circumstance. This re-use may have physiological benefits in
conjunction with apportionment of energy for other nesting activities,
because rapid location of a nest-site would mean that energy normally
expended in searching and selecting could be rechanneled for actual
construction. In each of the instances of rebuilding, the new nest
was begun on the same day that the previous nest was abandoned.
The re-nesting of pair 9 (1960) is worthy of note. These birds were
established in the elm thicket on Clark land. Elm was by far the most
abundant tree, with dogwood, Osage orange and honey locust also
relatively common. There were only six boxelders in the territory and
yet the four nests built by this pair were placed in them. This is the
only instance of seeming preference.
_Building_
Nestbuilding by Bell Vireos can be best discussed in terms of the
phases of construction described for the Red-eyed Vireo, Lawrence
(1953:57), which are: (1) construction of the suspension apparatus,
(2) construction of the bag, (3) lining of the bag and smoothing and
polishing of the exterior, and (4) adornment of the exterior. Red-eyes
(Lawrence, 1953:59) may continue adornment far into the period of
incubation. Both the male and female Bell Vireo have been observed to
add spider egg sacs and other silk to the exterior of the nest as late
as the sixth day of incubation.
Nice (1929:16) recorded only the female Bell Vireo building, but she
did recall, from previous studies, having seen males aiding somewhat.
Pitelka and Koestner (1942:102) wrongly concluded that the female Bell
Vireo builds unaided, but Hensley (1950:243) observed that both sexes
participated in nestbuilding, and Mumford (1952:229) reported two
instances of building by both adults. His description of the
activities viewed in mid-May suggest that they were of the
transitional period between the first and second phases. On the second
occasion he recorded both adults building during the second phase.
Since no details accompany this second observation I assume that it
pertained to activity not necessarily typical of this phase of
construction. Whereas both sexes of the Bell Vireo cooperate in
building the nest, only the female Red-eyed Vireo builds according to
Lawrence (1953:56). But Common (1934:242) saw both Red-eyed Vireos
building a nest.