Behavioral Ecology Vol. 9 No. 5: 515-524
Genetic monogamy in blue-headed vireos and
a comparison with a sympatric vireo with
extrapair paternity
Eugene S. Morton,* Bridget J. M. Stutchbury,b Joan S. Hewlett,0 and Walter H. Pipef1
"Conservation and Research Center, National Zoological Park, 1500 Remount Road, Front Royal, VA
22630, USA, b Department of Biology, York University, North York, Ontario, M3J 1P3, Canada, C3662
Kinter Hill Road, Edinboro, PA 16412, USA, and ^Molecular Genetics Laboratory, National Zoological
Park, Washington, DC 20008, USA
Based on the breeding synchrony hypothesis, we predicted, in two congeners that nest in similar habitat but differ in nesting
synchrony, that blue-headed vireos (Vireo solitarius) would have fewer extrapair fertilizations (EPFs) than red-eyed vireos (V.
oHvaceus). EPFs were rare in blue-headed vireos (1/37 nestlings), but common in red-eyed vireos (11/19 nestlings). We studied
the behavior of blue-headed vireos to determine what factors could promote genetic monogamy. We found no evidence that
males mate guarded to prevent extrapair copulations from occurring. Males did not follow fertile mates closely when mates left
the nest (14-25% of female departures) and, during the egg-laying period, males were often alone on the nest (22.3 min/h).
Female blue-headed vireos, but not red-eyed vireos, obtain direct benefits from social mates such as nest building and incubation
(49.1% of the total), and they assess male quality long before becoming fertile. Female blue-headed vireos spent more time
incubating when their mates had low incubation effort. Furthermore, male incubation effort was positively correlated with nest
survival during incubation. We discuss the evolution of genetic monogamy and sex role convergence in blue-headed vireos in
relation to asynchronous breeding. Key words: blue-headed vireo, breeding synchrony, DNA fingerprinting, genetic monogamy,
male incubation, mating systems, red-eyed vireo, sex roles, Vireo oHvaceus, VTreonidae, Vireo solitarius. [Behav Ecol 9:515—524
(1998)]
A
lthough the majority of birds are socially monogamous,
. genetic parentage studies have shown that social mo^
nogamy does not imply genetic monogamy (reviewed in Birkhead and Meller, 1992) because males and females often seek
and obtain extrapair copulations (EPCs) (e.g., Gibbs et al.,
1990; Gray, 1996; Kempenaers et al., 1992; Morton et al., 1990;
Neudorf et al., 1997; Wagner, 1991). Among songbirds, genetic monogamy is thought to be the exception rather than
the rule (Birkhead and Mailer, 1992), but there is great variation in the extent of extrapair fertilizations (EPFs).
In a comparative study, Stutchbury and Morton (1995) supported die breeding synchrony hypodiesis to explain this variation (see also Stutchbury et al., 1998). The hypothesis predicts that breeding synchrony is positively correlated widi EPF
frequency in passerine birds. They also snowed that songbirds
with long and asynchronous breeding seasons have small testes, an indirect measure of EPC frequency (Meller and Briskie, 1995), from which they hypothesized that asynchonoush/
nesting species would have low EPF frequencies. Recent DNA
fingerprinting studies on socially monogamous passerines
have confirmed that those with asynchronous nesting are genetically monogamous (Fleischer et aL, 1994,1997; Robertson
and Kikkawa, 1994).
The mechanism underlying the synchrony hypothesis highlights female control of die occurrence and evolution of EPFs.
Synchronization of female fertile periods within a population
creates conditions similar to leks, where females choose cop-
Address correspondence to E. S. Morton. E-mail: nzpem0349
srvmji.cdu. W. H. Piper is currently at tLj Department of Biology,
George Mason University, Fairfax, VA 22030, USA.
Received 20 November 1997; accepted 5 April 1998.
O 1998 International Society for Behavioral Ecology
ulation partners among males who are displaying simultaneously (Stutchbury and Morton, 1995; Wagner, 1993,1998).
When breeding is not synchronized, males are not displaying
simultaneously under die same conditions of weather, food
availability, and other energetic demands that change with
nesting stage. Consequently, the expected benefits to females
of engaging in EPFs are lowered because high-quality genetic
mates cannot be identified reliably.
A test for a causative relation between synchronous breeding and die evolution of EPFs is to compare die genetic mating system of closely related species diat • differ in terms of
breeding synchrony (Stutchbury and Morton, 1995). Here, we
compared die genetic mating systems of two such species, die
blue-headed vireo (Vireo solitarius; formerly called the solitary
vireo, Anonymous, 1997) and red-eyed vireo (V. oUvaceus).
These breed togedier in similar habitat on our study site but
differ in breeding synchrony. Bodi species are sexually monomorphic and both are long-distance migrants. Blue-headed
vireos are among die first migrants to return to our study site
in die spring (mid-April), and males remain on dieir territories until late September or early October (diis study). This
early arrival and long breeding season, along widi high predation, produces asynchronous nesting. In contrast, red-eyed
vireos arrive in mid- to late May and leave dieir territories by
late July, resulting in relatively synchronous nesting. The synchrony hypodiesis predicts diat blue-headed vireos have few
EPFs relative to red-eyed vireos.
We show diat red-eyed vireos do, indeed, have high breeding synchrony and many EPFs, whereas EPFs in blue-headed
vireos are even less common dian expected from dieir low
breeding synchrony. Widi this as a starting point, we focus on
possible ecological or behavioral factors underlying genetic
monogamy in blue-headed vireos.
516
METHODS
This study was conducted from April to August for 3 years in
northwestern Pennsylvania, USA (41° N, 79° W). The study
site is a 150-ha continuous, mixed hardwood forest that supports about 25 breeding pairs of bhie-headed vireo (BHVs)
and 75 red-eyed vireo (REV) territories. Adults were captured
with mist nets and banded with U.S. Fish and Wildlife bands
and color bands. We captured adults either at the nest during
the incubation or nestling stage or captured males away from
the nest using playback of song. We identified females based
on the presence of a full brood patch. Females do not sing in
either species.
In 1996 we identified previously color-banded male BHVs
as they arrived on breeding territories and banded new males
as they arrived. We conducted daily observations of interactions, changes in territory size, and pair formation behavior.
For six males, on adjoining territories in 20 ha of our study
site, we performed 2-h daUy observations of pair formation
behavior from male arrival until pairing.
Nests were located at the building, egg-laying, or incubation
stages, usually by following males and females to the nest
Male BHVs often gave a short, repetitive, and individually distinctive "nest song" when approaching the nest during die
building, incubation, and nestling stages (Figure 1). This nest
song is not present in REVs. Frequent observations and playback of song confirmed the identity of singing males on territories. In 1994 and 1995, we collected 30-100 uJ of blood
from adults and nestlings for use in DNA fingerprinting. In
1994 we discovered that female BHVs often abandoned their
broods if they observed us removing nestlings from die nest
for banding. In 1995 we captured both parents before handling nestlings and held them for 15-30 min in paper bags
while we took blood samples from nestlings. This procedure
eliminated any further cases of nest abandonment in BHVs.
We used video cameras or direct observation to confirm die
identity of die parental BHV male at all nests. The social father of a brood was denned as the male defending die territory during egg laying and who incubated eggs and cared for
die young. The social modier was die female who cared for
the eggs and nestlings.
In 1995 we also searched for REV nests to compare die
genetic mating system of die two congeneric species. The
same methods were used for collecting blood samples and
identifying die social parents. REV females did not abandon
nests when nestlings were handled.
We used a synchrony index (Kempenaers, 1993) to quantify
die degree of overlap in fertile period among females. The
index for a given female is die average percentage of females
in die population diat were fertile on die same days that particular female was fertile. The fertile period for a female was
conservatively denned as die period 5 days before laying die
first egg to the laying of die penultimate egg in die dutch
(Birkhead, 1992; Birkhead et aL, 1989).
DNA fingerprinting
Multilocus DNA fingerprinting was performed for 37 BHV
and 19 REV nestlings. Blood, stored at 4°C in phosphate-buffered saline/EDTA, was incubated overnight with proteinase
K, extracted with phenol and chloroform/isoamyl alcohol,
and dialyzed against 1XTE to produce dean, genomic DNA.
We then digested 5 peg of DNA widi HtuTR fer each individual
and ran digested DNA for 40 h at 48 V dirough 0.8% agarose
gels. In all cases, nesdings were run on die same gel with
social parents and neighboring males for which DNA was
available. We dien vacuum-transferred DNA from gels to nylon membranes (Magna Charge, Micron Separations, Inc.),
Behavioral Ecology Vol. 9 No. 5
UV-cross-linked DNA to die membrane, and hybridized membranes widi "P-labeled Jeffrey's probe 33.15.
We scored nesdings for parentage using novel bands (diose
not shared widi eidier social parent) and band-sharing coefficients (an index of shared DNA fragments; see Wetton et aL,
1987). The average number of fragments scored per lane was
16.4 ± 0.44 (n = 66) for BHVs and 15.1 ± 0.84 (n - 30) for
REVs. For BHVs, die band-sharing coefficient between unrelated individuals (social mates) was 0.20 ± 0.04 (N =• 11
pairs), giving an upper 95% confidence interval (one tailed)
of 0.41 for unrelated individuals. A nesding was defined as an
extrapair young if it had two or more novel bands, a high
band-sharing coefficient (>0.41) widi its social modier, and a
low band-sharing coefficient (^0.41) widi its social fadier (see
Figures 3 and 4). We had no fingerprint from die social
modier for an additional 5 BHV and 11 REV nesdings, so
parentage was assigned based only on band-sharing coefficient
widi die social fadier.
Nesdings determined to be extrapair young (i.e., die social
male excluded as die genetic fadier) were tested for parentage widi neighboring males run on die same gel, dirough
novel band and band-sharing analysis. True genetic fathers of
extrapair young were identified using die same parentage criteria.
Mate guarding and male parental effort
REV males do not build nests or incubate (Southern, 1958;
Morton et aL, personal observations), so we concentrated on
male BHV parental effort during die prehatching stages. For
behavioral observations on BHVs, we ensured diat at least one
member was color banded. For pairs diat were constructing
nests or laying eggs, we conducted two or diree 1-h watches
per pair to determine die extent to which males assisted widi
nest building and followed their mates closely during their
fertile period. We observed 16 different pairs and obtained
45 h of observation at die nest building, prelaying, and laying
stages. Prelaying was denned as die period 1-3 days before
die first egg was laid, and nest building was denned as die
period of active nest construction before die prelaying period.
For REVs, we observed eight pairs on contiguous territories
for 2 h each (16 h total) during die morning during die nestbuilding and egg-laying stages. We looked for evidence of
mate guarding, intruder pressure, and female copulatory behavior.
We used video cameras (placed 2-5 m from die nest) or
direct observation to document die degree of parental effort
by male BHVs at die incubation and nesding stages. At each
nest stage, we obtained 3-7 h of observations over a period
of 3-6 days, and usually between 0800 and 1400 h Eastern
Standard Time. We conducted feeding observations when
nesdings were at least 7 days old. We observed 25 different
pairs for a total of 181 h during die incubation and nesding
stages.
To obtain anodier measure of parental effort for maW, we
quantified die role of males in nest defense by presenting a
model of a nest predator, die blue jay (Cyanocitta cristata), at
BHV nests. In 1996, a covered blue jay model mounted on a
2.5-m pole was placed about 3 m from die nest on days 6-10
of die nestling stage. Trials were done using only those nests
< 3 m off die ground, so die model was approximately at nest
height. The cover was removed from die blue jay, dien two
ebsorws quaaaiiod tho Hnpesse to tfas blue jay for 10 min.
One person used a video camera while die odier dictated observations into a tape recorder.
Nonparametric statistics were performed using Statview 4.1
on a Macintosh computer. Means are reported with standard
errors.
Morton et aL • Monogamy in blue-headed vireos
517
(b)M-9
8 r-
(a) M-9
8 r-
6
kHz
4
0
0
(c) F-ll
(d) G-10
8 r-
8
kHz
1
4
2
•
1
0
(e) J-10
8 r-
(f) Fann
8 r-
kHz
1
Time (s)
1
Time (s)
Figure 1
Spectrograms of nest songs of five blue-headed vireo males showing individual distinctiveness. Nest songs consisted of one (n » 20 males),
two (n « 4; e.g., M-9), or three phrases (n = 1). Nest songs with similar phrases often differed in firequency range (e.g., males G-10 and
Farm).
518
Behavioral Ecology Vol. 9 No: 5
•
r-
BHV
a REV
o
.1 1.
11
May
18
8
June
15
.I
22
~l
29
6
July
1
Figure 2
Frequency distribution of first-egg dates for blue-headed (BHV; n
38 nests) and red-eyed (REV; n =» 15 nests) vireos in 1995.
1
2
First Egg Date
1
3
1
4
Novel bands
b) Social Father
RESULTS
Srteatng synchrony
The breeding synchrony index averaged 25 ± 1.5% for all
BHV nest initiations in 1995 (n = 39), and the range of first
egg dates was 6 May-5 July (Figure 2). Males were present
and singing on their territories from mid-April to mid-October. Many (18/37) nests were depredated, and 5-10% of pairs
were double brooded, so there was no sharp peak in breeding
activity (Figure 2). The degree of breeding synchrony in BHVs
varied among years. In 1994 first-egg dates ranged from 26
April to 7 Jury, and the synchrony index was 19.7 ± 4.6% (n
= 15 nests), comparable to 1995.
REVs were present and singing on their territories from
mid-May through late July. There was a sharp peak in nesting
activity in late May and early June as females began egg laving
(Figure 2). The breeding synchrony index averaged 43 ±
0.5% for all REV nests in 1995 (n = 15), which was significantly higher than BHVs (Mann-Whitney t/test, Z = 4.01, n
•=• 46, p < .0001).
Genetic mating system
All breeding adults were socially monogamous in both the
vireo species. Their genetic mating system, however, differed
dramatically.
All BHV nestlings but one were the genetic offspring of
their social parents (Figure 3a,b). EPFs accounted for only 1 /
37 (2.7%) nestlings and 1/16 (6.2%) broods. No intraspecific
brood parasitism was detected. The mean band-sharing coefficient between social fathers and their genetic young was 0.60
± 0.02 (n =» 36). The one extrapair offspring occurred in a
second brood, and the social father was the same male for
both broods. The identity of the genetic father of this extrapair young is unknown.
In REVs, 11 of 19 nestlings (58%) were the result of EPFs
(Figure 4), and 4 of 7 broods contained extrapair young.
Again, no instances of intraspecific brood parasitism occurred. The mean band-sharing coefficient between social fathers and their genetic young was 0.65 ± 0.04 (n = 8), and
0.24 ± 0.02 (n — 11) for extrapair young.
There was a significant difference between blue-headed and
red-eyed vireos in both the frequency of extrapair young
(Fisher's Exact test, p < .0001) and the frequency of broods
with extrapair young (/> ™ .017).
Pairing in BHVs m relation to territory she and arrival time
Female BHVs paired first with males holding the largest territories (Table 1; r, = - 3 8 2 , p < .04, n ~ 13). The earliest
arriving males did not hold the largest territories (r, *• —.311,
o
1
0
1
2
1
1
3
1
4
5
6
Novel bands
Figure 3
Number of novel bands for each blue-headed vireo nestling (n =
32) and proportion of bands shared with the (a) social mother and
(b) social Either. Dashed lines indicate cutoff points for excluding
parentage. There were five additional nestlings (from three
families) for which novel bands were not known because the social
mother was not sampled. These nestlings were categorized as
within-pair young because band sharing with the social male was
above 0.41 (range 0.46-0.74, mean = 0.61, SE = 0.04).
p < .25, n = 15), nor did days to pairing correlate with arrival
date (r, = .388, p < .18, n = 10). Four of the six neighboring
males observed intensively (Table 1: NG-J10, NG-M9, Farm,
NGJ1S, NG-C10, NG-F11) arrived on 18 April 1996; all six
males had arrived by 27 April. Males defended large territories at this time, much larger than areas used at the nesting
stage, which included hemlocks (Tsuga canadensis). The first
female was sighted 22 April and' formed a pair bond on that
day with male NG-J10, who defended the largest territory. She
associated with male NG-M9 and NG-J10 during the same day,
and intense male competition among the five males then present (NG-J10, NG-M9, NG-J13, NG-C10 and NG-F14), including
chases as well as intense singing characteristic of border clashes (James, 1978), was caused directly by her behavior of ignoring boundaries and bringing males into contact at their
territory borders. Males used their individual nest songs (Figure 1) abundantly when consorting with females and made
ritualized nest-building motions (James, 1978) only on hemlock branches, which was the only tree species with leaves at
tbis «Hao ef year.
Among the five males, NGJ10, who defended a large area
before female arrival (6.5 ha), won most border conflicts. NGJlO's territory shrunk to 2.0 ha when a nest site had been
selected in mid-May. Territories of three odier pairs were partly or wholly within his former defended area. Two pairs of
519
Morton et al. • Monogamy in blue-headed vireos
Tablel
Male arrival time, teifituiy m e , and number of days after arrival to
pairing and egg laying of bhie-headed vireo*
a) Social Mother
0.8
Arrival
date
Territory
(month/day) size (ha)
Male
2
3
NG-J10NG-M9*
Farm"
Farm"
NG-J13
NG-C10
W-12
S-16*
Y-13*
NG-F14
F-4
N&C15*
NG-F11*
M-19
E-13
NG-C10
4
Move) bands
b) Social Father
0.8
0.7 <>•
0.6
4/18
4/18
4/18
4/18
4/18
4/18
4/18
4/19
4/19
4/22
4/27
4/27
4/27
4/29
5/5
6.5
53
2.0
2.5
2.3
1.5
5.0
73
2.0
13
4.0
13
2.6
3.5
3.0
2.0
Days to
pairing
Days to
first egg
4
5
37
30
?
11
10
4
4
16
9
15
6
12
9
6
?
50
34
35
35
21
34
31
28
31
25
?
24
20
0.5
* Males banded in previous years, remaining males new in 1996.
Farm male is listed twice because he changed territories after arrival
(see text).
0.4
b
8
0.3
0.2
8
0.1
0
0
1
2
3
4
5
6
Novel bands
Figure 4
Number of novel bands for each red-eyed vireo nettling (n = 8)
and proportion of bands shared with the (a) social mother and (b)
social father. Dashed lines indicate cutoff points for excluding
parentage. There were 13 additional nestlings for which novel
bands were not known because the social mother was not sampled.
Seven of these nestlings (from two families) were categorized as
within-pair young because band sharing with the social male was
>0.41 (range 0.43-0.80, mean - 0.64, SE = 0.05). Four nesdings
(from one familiy) were categorized as extrapair young because
band sharing with the social male was <041 (range 0.20-035, mean
«=• 0.25, SE = 0.03).
birds new to the area (i.e., unhanded), moved into areas defended earlier by male NG-J10. One (Farm) abandoned a territory off the study site, where he had remained unpaired,
and moved 400 m to nest within NGJIO's former territory.
When he paired was not known. None of the pairs from previous breeding seasons re-formed, even if both individuals
were known to be present on the study site.
Females aggressively defend against intrusions by other females. Females have a distictive "whinny" vocalization given
mainly during female-female confrontations at this stage of
pair formation and nesting when females are still arriving on
the study site. Thus, later arriving females cannot easily move
among territories to compare males.
To summarize, males, upon arrival, defend areas larger
than those used when nesting. Females choose those males
with the largest territories first.
Mate guarding
One possible explanation for the low frequency of extrapair
matings in BHVs could be mate guarding by males. We observed the time male and female BHVs spent at the nest during the fertile stage and the frequency of female nest departures in which males followed their mate closely. Unlike other
studies of mate guarding (e.g., Beasley, 1996), we could not
compare male following behavior during the fertile versus
nonfertile incubation stages because males incubate the eggs
while females are off the nest (see below). If mate guarding
is important, however, then males should associate most closely with females during the prelaying and laying stages compared with the nest building stage, 4-10 days before egg laying, when copulations are less likely to result in fertilizations
(Birkhead, 1992; Birkhead et al., 1989).
The time females spent alone at the nest did not vary significantly (Kruskal-Wallis Test, H = 1.32, df = 2, p = .51) over
the nesting stages (nest building, prelaying, and laying; Figure
5), although time alone was highest (14.4 ± 4.8 min/h) during the laying stage. Males spent little time alone at the nest
during building and prelaying (1.5-2.0 min/h), but this in30
Female Atone
25
Male Alone
Pair Near/Together
nest buBding
prelaying
laying
Figure 5
Mean ( i S E ) time that male and female blue-headed vireo* spent
alone at the nest per hour and time the pair was together near
(<15 m) or at the nest during the nest building (n ~ 9 pain),
prelaying (n *> 10) and laying (n = 7) stages.
Behavioral Ecology Vol. 9 No. 5
520
nest building
preteying
laying
Figure 6
Frequency of female blue-headed vireo nest departures in which the
female left alone, was followed closely by her mate, or was not
followed but her mate was within 15 m of nest at the nest building
(n - 150 departures), prelaying (n — 28), and laying (n - 10)
stages.
creased significantly (H = 7.18, df = 2, p = .03) during the
laying stage (22.3 ± 5.5 min/h). To be conservative, we considered that males could guard their mates when females were
alone at the nest but the male was nearby (<15 m) and
lumped this category with the time the pair was together at
the nest The time the pair was together at or near the nest
did not increase significantly {H = 1.35, df = 2, p = 31) as
females approached the laying stage (Figure 5).
Another measure of mate guarding is the frequency with
which males closely follow their mates (<5 m) when they
leave the nest. During nest building, females were followed
closely in 14 ± 6.5% (n » 9 pairs) of nest departures, and
females departed alone in 71 ± 8.6% of departures. For 15
± 7.9% of departures, females were not followed closely, but
the male was within 15 m of the nest, so he could potentially
guard his mate without direct following. Females and males
visited the nest relatively infrequently during prelaying and
laying; thus too few nest departures were observed per pair
during these nest stages to calculate an accurate percentage
of sips fallowed. Thorafere, to compare male following behavior at different nest stages, we used a contingency table
analysis, even though individual departures were not strictly
independent The frequency of female departures from the
nest in which they were alone, were followed, or for which
the male was nearby (Figure 6) varied significantly with nest
stage (G test G = 14.7, df - 4, p < .01). Males followed their
mates most often during the prelaying stage, and there was
also a relatively high frequency of female departures where
the male was close to the nest but did not follow. During the
laying stage, however, males did not associate closely with females near the nest (Figure 6).
Intrusions and copulations
Territorial intrusions by neighboring BHV males were relatively uncommon, although males often countewang near territory boundaries. During the nest-building stage, we observed six intrusions during 19 h of observation (0.3/h). In
coasast, ws observed only one intrusion during 17 b. of prelaying observation and no intrusions during 9 h at the laying
stage. During intrusions males typically perched in close proximity (<10 m), singing at each other, and repeatedly displaced or chased each other. In only one instance did the
intruder male approach the resident female, and she flew rap-
idly away. The resident and intruder male (a color-banded
neighbor) fought in the air and fell, grappling, 10 m to the
ground.
We observed no EPCs and eight within-pair copulations:
three during nest building (0.15/h) and five during prelaying
(0.29/h). Although we could observe vireos as far as 30 m
from their nests during our nest watches, these copulations
all occurred close to, or on, the nest (4 ± 1.3 m away, range
0-10 m). In the six cases of successful mounting, the female
usually gave a solicitation display (five of six cases) to the male
who was perched nearby. He then gave either a quiet nest
song (n = 1) or "fast" courtship song (James, 1978; n = 5)
for 10-15 s, then immediately mounted the female. In the two
other cases the female rejected the copulation attempt by bill
snapping at her mate and giving harsh chatter calls. In both
these cases the female had not performed a copulation solicitation display, and the male gave no song immediately beforehand.
In red-eyed vireos, male intrusions were observed one to
two times per hour (n = 16 h) during late nest building in
eight pairs. Intrusions in REVs are common compared to
BHVs, but they were difficult to quantify because females
sometimes flew away from mates, initiating chase flights (see
Hoi, 1997). During chase flights, territorial boundaries were
not evident, so it was difficult to classify several chasing males
as "intruders." At this nesting stage, male REVs followed their
mates closely. Females were highly vocal when approached by
males, producing a harsh, short series of chatters when approached by their mates. This vocalization often immediately
followed a male's quick approach to a female accompanied
by a short (<2 s) song. It appeared to be a rejection of a
copulation attempt or a sex recognition vocalization, or both.
The female chatter was useful in detecting die presence of a
female on a territory during the female arrival period and in
locating the female during observations later. When female
REVs were nest building, their mates were mainly silent except for the short song given while approaching the female.
Male REVi accompanied their mates closely and attacked intruding males.
Malt partnial effort
BHV males were involved in all aspects of nesting (nest construction, incubation, feeding, brooding, nest defense), except egg laying. Males made 24.3 ± 7.2 % of nest-building
trips (n » 9 pairs) and spent 22.3 ± 5.5 min/h on die nest
during the egg-laying stage (Figure 5). REV males were involved only in feeding and nest defense, so the following data
pertain only to the BHV.
During the incubation period, males spent 27.9 ± 2.0 min/
h on the nest compared with 29.3 ± 2.1 min/h for their mates
(n • 24 pairs). Thus, males performed 49.1 + 3.8% of the
incubation duties. Together, the pair incubated the eggs for
57.3 ± 0.9 min/h, so the eggs remained covered virtually all
the time. There were nine pairs that never left their nest uncovered during 48 h of observation. For all pairs, the exchange at the nest usually took only seconds, preceded by call
notes and (if the female was on die nest) nest song by the
male as he approached the nest
There was extensive variation among males in their incubation effort, ranging from 14J>% to 100% of the total incubation performed. This had a large impact on female incubation effort because the time males spent incubating was
negatively correlated with the time their mates were on the
nest (Spearman rank correlation, r, • -.93, n » 24, p <
.0001). Male incubation effort (percent peformed by male)
was not significantly correlated with die total time the eggs
were incubated (r, « -.04, p - .85). Male incubation effort
did not differ during the incubation stage. The percentage of
Morton et al. • Monogamy in blue-headed vireos
100
521
Table!
Response of blue-beaded vireos to a Une Jay model placed near the
nest at the nrstHng stage (• » 9 pain). Paired attacks were those
where the male and female attacked in close tnfTrnhrn (within
several seconds of each other)
r
80
60
40
20
10
15
20
25
30
Nest survival (d)
Figure 7
Percentage of incubation performed by male blue-headed vireos
versus the number of days the nest survived (day 1 isfirstday of
incubation). Eggs hatched at 14 days, and nestlings fledged at SO
days.
time males incubated did not vary with day of incubation (r,
= -.037, n =» 14, p < .89). Females compensated for low male
incubation effort by increasing their own time on the nest
Time of day might be expected to affect male incubation effort, due to colder temperatures during the morning hours
(Smith and Montgomerie, 1992). However, for observations
made from early May to mid-June (when early mornings were
usually cold), there was no correlation between the amount
of time males incubated (min/h) and time of day (r, = .17,
n = 69 observations, p =• .17).
Male incubation effort affected nesting success (Figure 7).
Male incubation effort (percent performed by male) was significantly correlated with the number of days the nest survived
(r, = .40, n = 24, p = .05). Nests depredated during incubation were those where males had relatively low incubation
effort (Figure 7). Male incubation effort had a strong effect
on the number of days during incubation that the nest survived (r, «• M, p = .009). Male incubation effort did not
correlate with hatching success (percentage of eggs that
hatched) for nests that escaped predation (r, = - . 0 8 , n «* 15,
p = .77). For those nests that hatched, male incubation effort
also did not correlate with subsequent nestling survival (r, =
- . 0 5 , n = 18, p = .84). Most of these nest losses during the
nestling stage (Figure 7) were due to predation, but several
nests failed late in the nestling stage due to female abandonment (n = 4) or mite infestation (n •• 1).
During the nestling stage, males made 51.6 ± 3.4% (range
36-78%) of feeding trips (n D 11 pairs). For pairs still brooding their young when observations were made (n *» 6 pairs),
males brooded young for 7.7 ± 3.0 min/h, compared with 7.9
± 1.0 m i n / h for their mates. There was no "gr^ftc?"* correlation between male feeding effort (percentage of trips by
male) and the number of days the nestlings survived (r, •
- . 2 4 , n =• ll,/>"* .44). There was also no correlation between
male incubation effort (percent time) and his feeding effort
(percent trips) at the same nest (r, = .30, n = 10 males, p =
.37).
BHV pairs often attacked bhie jays when they did not have
a nest. Therefore, it was not surprising that they were extremely aggressive toward blue jay models presented near active
nests (Table 2), although there was great variability among
pairs in the intensity of attack. Once the blue jay was- discov-
Response
Mean ± SE
Range
Time to first attack (min)
% Paired attacks
Attacks rate (no./min)
3.1 ± 0.65
80.3 ± 4.4
10.3 i 1.1
03-6.3
56-98
6.0-15.8
ered, most pairs repeatedly dove at the model for the remainder of the trial. Vireos struck the model's back in many of
these attacks and growled as they struck. They uttered rasps
continually between attacks. It was difficult to identify the sex
of the a narking bird because the attack rate was so high (one
attack every 6 s). However, the male and female often coordinated their attacks, diving in close succession at the model
from starting positions on opposites sides of, and above, the
jay model, then pausing before another paired attack. The
male participated in nest defense in all trials, and about 80%
of all attacks were paired.
DISCUSSION
Breeding synchrony and mating system
As predicted based on their asynchronous nesting, BHVs had
significandy fewer EPFs dran REVs (2.7% versus 58% extrapair
young). The single extrapair nestling identified for BHVs was
from a rare event in our population: a second nesting of a
pair that had already fledged a brood. BHVs are essentially
genetically monogamous, an unusual mating system for a
long-distance -migratory songbird (Stutchbury and Morton,
1995). This dramatic difference in mating system was documented for these congeners in similar habitat in the same
study site and years.
Breeding synchrony, such as occurs in REVs, could promote
extrapair matings for two reasons. First, males are expected
to compete most intensely for extrapair matings when many
females are fertile and participating in EPCs. Second, females
may be more likely to participate in EPCs when male-male
competition is intense and males are displaying simultaneously, thereby providing females with substantial cues for discriminating among males (Hasselquist et aL, 1996; Rempenaers et
al., 1992; Mulder and Magrath, 1994; Stutchbury and Morton,
1995). Female REVs not only obtained EPFs abundantly, but
they also initiated chase flights to compare males, as Hoi
(1997) described for bearded tits (Panurus bUrrndcus).
We suggest that asynchronous nesting, as in BHVs, makes
it so difficult for females to assess male quality that females
do not seek or accept EPCs, especially in species where females use behavioral cues in mate choice (e.g., Hasselquist et
aL, 1996). As a result, males should reduce or eliminate extrapair mating effort. Other temperate-zone songbirds with
comparable levels of breeding synchrony as the BHV (1725%) also tend to have a relatively low frequency of EPFs
(Stutchbury and Morton, 1995). The BHV has a low EPF frequency (2.7% young, 6.2% of broods).
It is possible that the correlation between breeding synchrony and EPF frequency can be explained by purely mechanistic hypotheses. For example, when pairs are synchronous,
everyone is seeking copulations, so perhaps EPFs will be higher. Under this hypothesis EPFs should correlate directly with
nesting synchrony but be distributed randomly among different nests or pairs. The distribution of EPFs is not random
(e.g., Hasselquist et al., 1996; Morton et al., 1990; Stutchbury
522
et al., 1994), so this mechanistic hypothesis can be rejected.
Breeding density is often thought to increase opportunities
for obtaining EPCs (Birkhead and MoOer, 1992; Westneat et
al., 1990), so density is a possible influence here because REVs
were three times more common than BHVs. However, breeding density does not correlate with EPF frequency across species (Westneat and Sherman, 1997), and many studies within
species have found no density effect (Dunn et al, 1994; Tarof
et al., 1998). Furthermore, density may increase as a result of
females seeking EPFs, not because of density (Wagner, 1993;
Stutchbury and Morton, 1995). Although BHVs bred at relatively low density, all females had two tofivecontiguous neighboring pairs, providing ample opportunity to seek EPCs. Territories were not isolated from one another. Lower breeding
density in BHVs appears due to a female preference to pair
with males having large territories (Table 1). Breeding density
is known not to affect EPF frequency on our study site in the
hooded warbler (WUsonia dtrina). Hooded warbler territories
isolated by distances greater than BHVs nevertheless had high
EPF frequencies (40% of broods) (Tarof et al., 1998). Although we cannot rule out a density effect in vireos, the weak
evidence for density effects in songbirds suggests that tome
other factor must be important
We discuss other alternative hypotheses elsewhere (Stutchbury, 1998). These include density and the rapid pair-formation hypothesis, which states that migratory species are more
likely to have EPFs because rapid pair formation constrains
the ability of females to assess the quality of social mates (Westneat et al., 1990). Below we consider two more fruitful alternative hypotheses to explain low EPF frequency in BHVs. The
first hypothesis is that male BHVs prevent their mates from
obtaining EPCs by close mate guarding during the fertile period (e.g., MacDougall-Shackelton et aL, 1996; Wagner et al.,
1996a). The second hypothesis is that female BHVs do not
seek EPCs because the indirect benefits that could be gained
from extrapair matings are minimal
Mate guarding and genetic monogamy
Numerous studies have shown that close mate guarding by
males can reduce the frequency of extrpair mating attempts
on their mate (Bjdrkland and Westman, 1983; Bjorkland et
aL, 1992; Birkhead et al., 1989; MacDougall-Shackelton et aL,
1996). Therefore, genetic monogamy in BHVs might result
from males being effective in preventing EPCs from occurring.
We can reject this hypothesis, however, because males rarely
guard their mates closely regardless of nesting stage. Our results showed that the time females spent alone at the nest did
not differ significantly over the nest building, prelaying, and
laying stage (Figure 5), and males followed their mates closely
during only 14-25% of nest departures (Figure 6). Males did
tend to associate more closely with the female and nest area
during the prelaying period (Figure 6). However, during the
laying stage males typically spent 22 min/h alone on the nest,
making it impossible for them to guard their mates. We conchide that females had ample opportunity to participate in
EPCs (see also Schldcher et aL, 1997).
The tendency for males to associate more closely with females and nests during the prelaying stage (Figure 6) could
result from increased opportunities for within-pair copulations. Most copulations that we observed occurred dining the
prelaying stage. Successful copulations occurred close to nest
( 1 0 m).
Female mate choice, direct benefits, and good genes
Given the absence of intense mate guarding by male BHVs,
females dearly had the opportunity to seek EPCs. However,
EPFs were rare, suggesting that females do not have an extra-
Behavioral Ecology Vol. 9 No. 5
pair mating tactic. Thus, in BHVs, female choice of social
mate is also a choice of a genetic mate. When male parental
care has a large effect on female fitness, females may choose
mates primarily for direct benefits (parental care) rather than
indirect benefits (good genes). This should be especially true
for species where males incubate because females rely on male
incubation effort for successful nesting (Bart and Tomes,
1989).
Ketterson and Nolan (1994) suggested that when females
benefit greatly from male incubation, female mate choice
should be based on cues that predict paternal behavior, rather
than exaggerated traits. What cues could a female BHV use
to predict male paternal care? In BHVs, male courtship behavior during pair formation involves aritulalizednest-building display when females are present, going through the motions of nest building but without nesting material (James,
1978; this study). This courtship display, which is absent in
REVs (Morton et aL personal observations), suggests that this
display of parental effort is important to females. Also, males
often begin nest building before obtaining a mate, and show
these nests to prospective mates (although these nest starts
are not subsequently used for breeding).
We found two lines of evidence suggesting that male parental effort in BHVs affects female fitness. First, females compensated for low incubation effort of males by spending more
time incubating, which presumably imposes some energetic
cost on the female. BHVs incubate the eggs virtually 100% of
the time, so any reduction in male incubation effort will immediately affect the female. Other studies of incubation in
passerines have also found that females have increased energy
or foraging time (Kleindorfer et al., 1995; Smith et al., 1995)
as a benefit of male incubation. Male incubation effort was
also correlated with nest survival during incubation (Figure
7) (see also Kleindorfer and Hoi, 1997). This could occur if
males with high incubation effort are also more effective at
defending the nest from predators. The predator presentation
trials during the nestling stage clearly indicated that males
play an important role in nest defense (Table 2) and that pair
members coordinate their attacks, possibly enhancing their
effectiveness against predators.
A second, and not mutually exclusive, possibility is that the
kinds of heritable traits that will benefit females in terms of
offspring quality require close and persistent observation of
male displays and can only be assessed in social mates. Female
BHVs depend greatly on male parental care. Accordingly,
male courtship displays involve ritualized parental behavior
always coupled with individually distinctive nest song (Figure
1). This suggests that a male's mating success is determined
primarily by bis ability to provide parental care (especially incubation) . A female responds to male ritualized parental behavior, for this is important to her reproductive success, and
the male's nest song conditions her to respond sexually to an
individual male. Parental performance may be an important
component of sexual selection but is often unrecognized
(Wagner etaL, 1996b).
In 1996 we studied the pairing process on six contiguous
territories from before the arrival of thefirstfemale until nesting. Male BHVs attempted to defend courtship territories that
were much larger than their post-pairing nesting territories.
When the earnest females arrived, they visited several males
during a single day. They cruised through territories and
brought males in direct confrontations at borders. Females
bmight about male-male confrontations, and their preferred
males were apparently those holding the largest territories
(Table 1). This female preference is likely the source of selection favoring an exaggerated territory size during female
mate choice and a relaxation of territorial effort during actual
nesting. It appears that, unlike most temperate zone passer-
Morton et aL • Monogamy in blue-headed vireos
ines with high Eft's, female BHVs compare males long before
becoming fertile.
In species with extrapair mating systems, it is still unclear
exactly how females benefit from EPCs, but getting good
genes (e.g., Hasselquist et aL, 1996; Kempenaers et aL, 1992;
Wagner, 1998) or genetic variation (Brown, 1997), especially
at the major histocompatibility locus (e.g., Davidar and Morton, 1993) are often mentioned. Female BHVs could possibly
seek EPCsfromneighbors to obtain good genes. For instance,
in other species females choose genetic mates based on traits
that indicate high survivorship, such as male age (Morton et
al., 1990) or song repertoire size (Hasselquist et al., 1996).
However, females cannot obtain genes for good parenting
from their social mate and good survival genes from a neighbor male. Thus females may face a trade-off in the value of
good genes they can obtain from their social mate versus extrapair mates. This idea is not independent of the effects of
asynchronous nesting. The benefits females could gain from
obtaining better genes for their offspring from neighboring
males will be devalued if females have difficulty assessing male
quality due to nesting asynchrony because males are not competing simultaneously and under the same conditions.
Few species exhibiting high rates of male incubation have
been DNAfingerprinted,but most have low levels of extrapair
paternity (Ketterson and Nolan, 1994; Miller and Birkhead,
1993). These species include the European starling (Sturnus
xndgaris, 8.7% extrapair young; Smith et al., 1995), the zebra
finch (Taeniopygia guttata, 2.4%; Birkhead et aL, 1990) and
die dusky antbird (Cercomacra tyrcmnina, 0%; Fleischer et aL,
1997), as well as the BHV.
The correlation between male incubation and low EPFs
might result from lost mating opportunities when males incubate (Ketterson and Nolan, 1994). This idea assumes* that
males face a trade-off between incubation effort and seeking
EPCs. Smith and Montgomerie (1992) suggest that male barn
swallows (Htrundo rustica) do not reduce incubation effort
when EPC opportunities are greatest because males can seek
EPCs without substantially reducing their contribution to incubation. Male hooded warblers only spend about 5 min/h
off of their territories in search of EPCs (Stutchbury, in press).
Although male hooded warblers do not incubate, this behavior does suggest that males do not face important time constraints in seeking EPCs. Thus, male songbirds should be able
to pursue EPCs and incubate.
An alternative view is that breeding asynchrony sets die
stage for male incubation because, in the absence of an extrapair mating system, sex roles are expected to converge
(Ketterson and Nolan, 1994; Morton, 1996). When females
do not seek or accept copulations from extrapair mates, males
will not invest time and effort in seeking EPCs because they
will not benefit from doing so. Male incubation should be
more likely to evolve in these species.
The species with low EPFs and incubating males (noted
above) also have relatively low breeding synchrony due to long
breeding seasons and multiple broods. Thus we cannot say
whether asynchrony, or male incubation, is the more important influence on the evolution of mating systems. Recently,
however, high levels of EPFs (19% of young, 35% of broods)
were found in the house martin (Dehchon urbica), a species
where males perform 50% of the incubation but breeding
synchrony is very high (Whittingham and Iifjeld, 1995). We
predict that other species with male incubation but high
breeding synchrony will also have an extrapair mating system.
If so, this suggests that breeding asynchrony sets the stage for
male incubation because, in the absence of an extrapair mating system, sex roles can converge. This suggests that breeding
synchrony is die leading cause favoring an EPF-based breeding system.
523
We thank A. Sangmeister for field assistance in collecting red-eyed
vireo data. We also thank A. J. Jeffreys for minisatellite probes and R.
Fleischer for hii collaboration in DNA fingerprinting. T. Pitcher, S.
Gill, and R. Wagner provided valuable comments on the manuscript
This research was supported by Friends of the National Zoo and the
Smithsonian Migratory Bird Center, a Smithsonian Institution Scholarly Studies grant, and a grant to BJ.M.S. from the Natural Sciences
and Engineering Research Council of Canada.
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