Behavioral Ecology Vol. 12 No. 5: 541-546
© 2001 International Society for Behavioral Ecology
The effectiveness of mate guarding by male black-throated blue warblers
a Department of Biological Sciences, the State University of New York at Buffalo, 109 Cooke Hall, Buffalo, NY 14260, USA b Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA
Address correspondence to M.S. Webster, who is now at the School of Biological Sciences, Washington State University, P.O. Box 644236, Pullman, WA 99164-4236, USA. E-mail: mwebster{at}wsu.edu . H.C. Chuang-Dobbs is now at the Biology Department, Southern Utah University, Cedar City, UT 84720, USA.
Received 10 January 2000; revised 22 September 2000; accepted 9 October 2000.
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ABSTRACT |
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In many socially monogamous birds, males maintain close proximity to their mates during the fertile period. This is often considered an effort on the male's part to prevent other males from copulating with his mate, but other functions have been suggested and the effectiveness of males in preventing extrapair fertilizations has come into question. Moreover, it is unclear whether mate guarding conflicts with other male activities, particularly the pursuit of extrapair fertilizations. We examined mate guarding by male black-throated blue warblers (Dendroica caerulescens). Behavioral observations showed that males that guarded their mates more closely were less likely to have extrapair young in their nests. Moreover, the experimental detention of a male for 1 h during the fertility risk period increased the probability that a brood would contain extrapair young. Thus, male mate guarding was effective in reducing the risk of extrapair fertilization. Males with many opportunities for extrapair copulations appeared to guard their mates less and consequently had more extrapair young in their broods than males with few such opportunities. This suggests that mate guarding may conflict with the pursuit of extrapair fertilizations.
Key words: black-throated blue warbler, breeding synchrony, extrapair paternity, mate guarding, microsatellites, time conflicts.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In socially monogamous birds, females often copulate with males other than their social mates. Such extrapair copulations (EPC) can result in extrapair fertilizations (EPF), and thereby reduce the reproductive success of the cuckolded male. We therefore expect males to adopt behaviors that prevent their mates from engaging in EPC (Parker, 1970
; Stockley,
1997). If, for instance, a male can remain near his mate and
physically prevent other males from copulating with her, then such mate
guarding could be strongly favored by selection. In a large number of species
males maintain close proximity to their mates during the female's fertile
period (i.e., the period during which her eggs can be fertilized), and this
behavior is often interpreted as mate guarding by males
(Birkhead, 1998).
The proposal that male birds guard their mates has generated some
controversy, which centers on three points. First, alternative explanations
have been proposed for the close association between males and females during
the fertile period (Birkhead and
Møller, 1992; Dickinson
and Leonard, 1996; Gowaty and
Pilssner, 1987). For example, males may be protecting their mates
from predators (e.g., by acting as sentinels), and such protection may be most
important during the egg laying period when female foraging demands are high.
Of those studies that have examined patterns of male attendance to his mate
(e.g., Dickinson and Leonard,
1996), most have concluded that males are indeed acting to prevent
EPC (reviewed in Birkhead,
1998).
Second, even if males do remain near their mates to prevent EPC, the
effectiveness of this strategy has been called into question
(Stutchbury and Neudorf,
1998). Time constraints may prevent males from effectively
guarding their mates during the entire fertile period, and females may often
adopt behaviors that circumvent male guarding efforts. Empirical studies
indicate that it may be relatively easy for a female to elude the mate
guarding efforts of her mate (Johnsen et
al., 1998; Kempenaers et al.,
1995; Stutchbury and Neudorf,
1998), and that the intensity of male mate guarding often is not
associated with level of EPF (e.g.,
Johnsen et al., 1998;
Kempenaers et al., 1995;
Riley et al., 1995;
Schleicher et al., 1997;
Wagner et al., 1996). Such
results have led to a discussion over which sex is in "control" of
fertilization
(Björklund et
al., 1992; Blakey and Norris,
1994; Lifjeld and Robertson,
1992; Osorio-Beristain and
Drummond, 1998; Stutchbury and
Neudorf, 1998; Wagner,
1991). Several experimental tests of mate guarding have shown that
EPC attempts increase when a male is prevented from guarding his mate
(reviewed in Birkhead, 1998).
However, most of these experiments have not examined paternity of nestlings,
so it is unclear whether increased EPC attempts lead to increased EPF
(Stutchbury and Neudorf,
1998). Moreover, in some experiments males were removed for long
periods of time, often days, leading to difficulties in interpreting results
(see Discussion).
Third, it is unclear whether male mate guarding conflicts with other
activities, and as such whether guarding is costly. For example, mate guarding
may reduce the amount of time that a male may devote to foraging or the
pursuit of EPC (Birkhead and Biggins,
1987; Westneat et al.,
1990). In the latter case, guarding males will either have to
forgo extrapair mating opportunities or reduce their own guarding efforts to
pursue EPC. If mate guarding incurs such costs, then it may be difficult for
some males (e.g., those in poor condition or those faced with many mating
opportunities) to guard their mates effectively. Alternatively, mate guarding
may not be a costly endeavor. For example, if EPC involves only short absences
from the territory (Stutchbury,
1998b; Westneat,
1994), it may be relatively easy for a male to both guard his
social mate and pursue EPC (Westneat and
Gray, 1998).
We studied a breeding population of black-throated blue warblers
(Dendroica caerulescens) at the Hubbard Brook Experimental Forest,
West Thornton, New Hampshire, USA. These birds are small (ca. 10 gms),
socially monogamous (Holmes,
1994), migratory passerines that breed from May until August in
our study area. Genetic analyses (Chuang
et al., 1999; Webster et al.,
2001) have demonstrated that EPF are common and affected by local
breeding synchrony in this population, but as of yet it is unclear whether
females pursue and/or benefit from EPF. In this study we combined field
observations and experimental manipulations with molecular genetic analyses of
paternity to examine the effectiveness of male mate guarding.
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METHODS |
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General field methods and behavioral observations
We collected behavioral observations and monitored breeding on a 100 ha study plot (the observation plot) at Hubbard Brook (see Webster et al., 2001
). All
adults breeding on this plot (n = 75 in 1998) were color banded for
individual identification. At the time of banding we collected a small (ca. 20
µl) blood sample for genetic analyses. We visited all nests on this plot
approximately once every 3 days. We banded and collected a blood sample from
all nestlings 6 days after they hatched.
Studies of sperm usage in birds (reviewed in
Birkhead and Møller,
1992) indicate that: (1) copulations occurring many days (10 or
more) before the first egg is laid can lead to successful fertilization, but
(2) most EPF arise from copulations occurring during a much more narrow window
of time, which we term the "fertility risk period." Males of most
species appear to concentrate their guarding efforts into this period when the
risk of EPF is highest (see Birkhead,
1998). For birds with infrequent EPC, the fertility risk period
appears to extend from day -2 to day 1 (where day 0 is the first egg day; see
Colegrave et al., 1995;
Lifjeld et al., 1997). For
species in which females frequently copulate with multiple males, the
fertility risk period may cover a slightly longer period, particularly by
extending through most of egg laying
(Briskie, 1992;
Davies et al., 1992). Because
EPF are common in our study population
(Webster et al., 2001), we
defined a female's fertility risk period (i.e., the period during which
copulations are most likely to result in EPF) as the period beginning three
days before the first egg of a clutch was laid, and ending the day the
penultimate egg was laid.
Levels of local synchrony were measured as the number of neighboring females (i.e., those on adjacent territories) whose fertility risk periods overlapped a focal female's by at least 1 day (only females with known neighbors were used for these analyses; territories at the edge of the study plot were excluded). A male was considered to be in an area of "low" local synchrony if his mate's fertility risk period overlapped that of three or fewer neighboring females, and in an area of "high" local synchrony if his mate's fertility risk period overlapped that of four or more neighbors (where 3.5 fertile neighbors was the population median in 1998).
For behavioral observations, we followed focal males (mean observation time = 38 min, range = 23 to 60 min) and recorded every instance that a male followed a female or vice versa, the frequency of chases and fights between males, and the amount of time males devoted to foraging and vigilance. In addition, during these observation periods we recorded the estimated distance between the male and female once every 2 min. Eleven males were followed before or during the egg laying period (nine during the fertility risk period and two during late nest building on day -5), and four males were followed during their mates' incubation period. We compared behaviors during these two periods by calculating an average measure (e.g., average number of chases/fights per min of observation) for each male. Sample sizes were smaller for comparisons of behavior with paternity (see results) because predation eliminated the broods of some focal males before young could be sampled.
Experimental removals
Removals were conducted in 1998 on a second study plot (the experimental
plot) less than one km from the observation plot. We captured males by
broadcasting a playback of taped male songs from a loudspeaker located next to
a mist net. The mean ± SD time from start of playback until capture was
37 ± 28 min (n = 16). All removals were conducted on day -1 or
0, where day 0 was the day the first egg was laid. We held each captured male
for 60 min in a small cage (kept on the territory, but covered with a cloth
and out of sight away from the nest) and supplied him with food (mealworms)
ad lib. After this confinement period the male was released back onto
his territory. We completed 16 removals on the experimental plot, but only
five of these experimental broods survived until the young were old enough for
us to collect a blood sample, reducing our sample sizes for paternity
assessments. An additional eight males were not captured, but responded to the
playback by flying into the area and countersinging with the tape. Broods for
three of these survived long enough for blood samples to be collected (the
other five were depredated). These three males spent an average of 130 min
(range 60-210) interacting with the tape rather than consorting with their
mates, and we therefore included them in the experimental treatment group.
Because all males responded aggressively to the playback and predation was
likely random with respect to treatment, these experimental nests represent an
unbiased sample. Eight additional broods on the experimental plot survived to
fledging, and the males associated with these nests were not exposed to song
playback nor captured during the female's fertility risk period. We compared
the frequency of EP young in these eight control broods to that in the eight
experimentals.
Genetic analyses of paternity
Microsatellite methods are detailed in Webster et al.
(2001). In brief, we isolated
DNA from individual blood samples by standard phenol/chloroform extractions.
For each individual, we amplified with polymerase chain reaction (PCR) a total
of five microsatellite loci using two pairs of primers isolated from the
genome of the yellow warbler (D. petechia), Dpµ 01 and
Dpµ 16 (Dawson et al.,
1997), and three pairs of primers isolated from the genome of
D. caerulescens (Webster et al.,
2001), Dca 24, Dca 28, and Dca 32. PCR
products were radiolabelled by incorporating 33-P dATP in the PCR reaction,
and PCR products were size-sorted by gel electrophoresis in a 6% denaturing
polyacrylamide gel. Dried gels were exposed to autoradiography film for 1-3
days. To determine the genotype of each individual at each locus, we scored
the position of bands by comparison to a size standard. Previous genetic
analyses indicated that intraspecific brood parasitism is rare in this
population (Chuang et al.,
1999), so we identified extrapair young (EP young) by comparing
the nestling's paternally-derived allele to the genotype of its social father
(i.e., the male that fed it at the nest). The number of alleles per locus
ranged from 11 to 30, observed heterozygosities were 0.49 to 0.94, and the
combined probability that a randomly selected male would possess a nestling's
paternal allele at all five loci (i.e., the probability of false inclusion,
calculated following Jamieson,
1994) was less than 0.0002.
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RESULTS |
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Paternity and male mate guarding
Microsatellite analyses of 147 nestlings from 42 broods on the observation plot during the 1998 breeding season showed that 35 (23.8%) were not sired by the female's social mate. This is a level of EPF similar to that observed for this population in other years (Webster et al., 2001
). Males and females were in close proximity to each other (< 20 m) for 49.5% of the scan samples collected during the fertility risk period. This close proximity appeared to be maintained by males, as they were more likely to follow females than the reverse during the female's fertility risk period (Wilcoxon signed-rank test, Z = 2.81, n = 11, p =.005; Table 1). Males spent less time foraging and vocalized more during the fertility risk period than during incubation, but other male behaviors we recorded did not differ between the two nesting periods (Table 1).
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Our two measures of mate guarding were correlated with each other (r =.791, n = 11, p =.002), and both were strongly associated with the probability that a brood would contain extrapair young: Males who followed their mates frequently and spent more time within 20 m of them had a low probability of having an extrapair nestling in their nests (Table 2 and Figure 1). Other behaviors measured were not associated with the presence of extrapair young (Table 2).
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Temporary male removal experiment
To test more directly the role of males in deterring EPF, we conducted a
temporary male removal experiment on a second study plot. All experimental
males were observed frequently on their territories after experimental
detention (i.e., during the remaining fertility risk period). The proportion
of control nests containing extrapair young did not differ from the proportion
of nests on the observation plot with extrapair young
(Figure 2; Fisher's exact test,
p =.459). In contrast, extrapair young were present in the nests of
all eight experimental males (Figure
2; experimental versus control nests: Fisher's exact test,
p =.039). The proportion of EP young ± SE was 0.729 ±
0.115 in experimental nests (n = 29 young in eight nests) versus
0.438 ± 0.175 in control nests (n = 26 young in eight nests).
Overall, experimental detention of a male increased the probability that his
brood would contain one or more extrapair nestling (likelihood ratio = 6.90,
p =.009).
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Mate guarding and local synchrony
Most extrapair young were sired by neighboring males in this study
population (Webster et al.,
2001), so the number of fertile females on neighboring territories
is an indicator of a male's extrapair mating opportunities. The rate at which
males followed their mates was negatively associated with the number of
fertile female neighbors (Kendall's 
= -0.61, n = 8, p
=.01; three focal males at edge of study plot excluded from analysis), such
that males in areas of high local breeding synchrony (see Methods) followed
their mates less than males in areas of low local synchrony
(Figure 3). Similarly, the
number of fertile female neighbors was negatively associated with the amount
of time males spent within 20 m of their mates (Kendall's = -0.607,
n = 8 males, p =.02). Finally, in agreement with previous
studies of this species (Chuang et al.,
1999), the probability that a male's nest would contain EP young
was positively associated with the number of female neighbors that were
fertile at the same time as the male's mate (analysis using all males on the
observation plot except those with edge territories, n = 17,
likelihood ratio = 3.81, p =.05). These results suggest that males in
this population may reduce guarding and sacrifice some paternity in order to
pursue copulations with neighboring females (see Discussion).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The effectiveness of male mate guarding
Like males of many other passerine species, male black-throated blue warblers maintain close proximity to their social partners during the female's fertility risk period (see above and Holmes, 1994
). Most behavioral
and observational studies of this behavior (reviewed in
Birkhead, 1998) support the
hypothesis that it functions to prevent EPC: By remaining near his mate, a
male is able to physically prevent other males from approaching and copulating
with her. However, the effectiveness of such mate guarding in preventing EPF
is unclear. First, behavioral observations suggest that unguarded females are
able to reject unwanted EPC in many species (e.g.,
Björklund et
al., 1992). Although this suggests that not all unguarded females
will engage in EPC, some females may nevertheless do so, and every nestling
sired by an extrapair male represents lost reproduction for the female's
social partner. Therefore, observations of female rejection of EPC do not
reject the hypothesis that mate guarding functions to prevent EPF.
Second, it may be relatively easy for females to evade the mate guarding
efforts of their mates, such that those seeking EPC may be successful
regardless of male behavior (Chek and
Robertson, 1994; Gray,
1996; Johnsen et al.,
1998; Wagner et al.,
1996). This is particularly true given that a single welltimed
copulation can fertilize several young
(Birkhead and Møller,
1992; Colegrave et al.,
1995), and some evidence suggests that males deliver unusually
large levels of sperm during EPC (Birkhead
and Fletcher, 1995; Birkhead et al.,
1994,
1995;
Birkhead and Petrie, 1995).
However, relatively few studies have been conducted to examine female efforts
to obtain EPC (Double and Cockburn,
2000; Kempenaers et al.,
1995; Neudorf et al.,
1998; Smith,
1988), and it is currently unclear how easily females can evade
their mates in most species (see Gowaty,
1996).
We found a negative relationship between the intensity of male mate
guarding and the probability that a brood would contain extrapair young,
supporting the hypothesis that mate guarding reduces EPF. However, several
other studies have not found such a relationship
(Gowaty and Bridges, 1991;
Johnsen et al., 1998;
Kempenaers et al., 1995;
Krokene et al., 1996;
Riley et al., 1995;
Schleicher et al., 1997;
Wagner et al., 1996),
suggesting that male mate guarding may be ineffective at deterring EPF in at
least some species. Observational evidence for mate guarding, though, can be
confounded by other factors, particularly individual quality if it affects a
male's ability to guard or a female's ability to evade its mate (for
discussion, see Gowaty, 1996;
Lifjeld et al., 1994). For
this reason an examination of the function of mate guarding requires
experimental testing
(Björklund
and Westman, 1983; Komdeur et
al., 1999; Krokene et al.,
1996; Møller,
1987b).
The results of our male detention experiment are unlikely to have been
influenced by male or female quality, because pairs were assigned to treatment
groups at random (see Methods). This experiment showed that males of this
population are able to reduce, but not eliminate, EPF when allowed to remain
near their mates during the fertility risk period. Moreover, we detained
experimental males for only 1 h, because longer periods of detection may make
it difficult to distinguish extrapair fertilizations from mate replacement
(Blakey and Norris, 1994). The
short period of time that we detained males, combined with a previous
experiment with this species showing that mate replacement requires up to 3
days (Marra and Holmes, 1997),
make mate replacement an unlikely explanation for our results.
Several other experimental studies have demonstrated that guarding reduces
extrapair copulation attempts (see review in
Birkhead, 1998), and two of
these used procedures similar to our own (i.e., a 1 h detention). First,
Westneat (1994) found that a 1
h detention of male red-winged blackbirds (Agelaius phoeniceus)
increased the probability of EPF if that detention occurred near egg-laying.
Second, Dickinson (1997)
showed that a 1-h detention of male western bluebirds (Sialia
mexicana) increased both extrapair intrusions and EPC rates (parentage
was not assessed). In a somewhat different approach, Komdeur et al.
(1999) experimentally induced
male Seychelles warblers (Acrocephalus sechellensis) to stop mate
guarding (by introducing eggs to the nest rather than by male detention), and
found that the rate of successful EPC increased in the non-guarding
experimental group. Although Komdeur et al. did not assess parentage, the
experimental protocol eliminated alternative explanations and therefore
strongly supported the mate guarding hypothesis.
Thus, our results contribute to a growing body of evidence showing that
males of at least some species can reduce the probability of EPC/EPF by
guarding their mates. This does not indicate that males are in
"control" of fertilization in these species, as females may adopt
behaviors to partially circumvent male mate guarding, and may also be able to
reject copulation attempts by undesirable suitors. In the end, the probability
that a brood will contain extrapair young is likely to be influenced by
behaviors adopted by both sexes (Gowaty,
1996). These results also suggest that, in addition to the
possibilities of sperm depletion and sexually transmitted diseases, one cost
of EPC effort may be that males leave their mates open to the EPC attempts of
other males. This cost may be high in synchronous populations (see below) and
possibly those that nest at high density.
Mate guarding and reproductive synchrony
Our results have some bearing on the current controversy regarding the
effects of ecological and social factors
(Petrie and Kempenaers, 1998;
Westneat et al., 1990),
particularly breeding synchrony
(Schwagmeyer and Ketterson,
1999; Stutchbury,
1998c; Weatherhead and
Yezerinac, 1998), on female breeding behavior and EPF. A positive
correlation between population breeding synchrony and EPF frequency appears to
hold across species (Stutchbury,
1998a,c),
and a similar positive association between local breeding synchrony and EPF
was found in our study population (Chuang
et al., 1999). One possible explanation for such a relationship is
that breeding synchrony facilitates the ability of females to compare and
choose among extrapair males (Stutchbury
and Morton, 1995; Stutchbury
and Neudorf, 1998).
An alternative, but not mutually exclusive, explanation is based on the
premise that it is difficult for a male to both guard his mate and pursue EPF.
Although such a trade-off is usually expected to create a negative correlation
between synchrony and EPF (Birkhead and
Biggins, 1987; Westneat et
al., 1990), a positive correlation would result if males faced
with many fertile females reduce mate guarding in order to pursue copulations
with those females. This hypothesis assumes that a male's ability to guard his
mate will be affected by time allocated to other activities (see
Hasselquist and Bensch, 1991;
Westneat, 1994), and that
males can monitor the reproductive status of neighboring females (see
Magrath and Elgar, 1997;
Møller, 1987a;
Westneat, 1988). In our study
population, males faced with many opportunities for EPF (i.e., many fertile
neighbor females) appeared to guard their mates less than males with few such
opportunities, and consequently were more likely to have extrapair young in
their broods (see also Chuang et al.,
1999).
These possibilities require further testing. First, it is not clear what cues females of most species use to choose extrapair mates, nor how these cues might be affected by breeding synchrony. Similarly, it is generally unknown how synchrony affects male and female behavior (e.g., forays off the territory and displays to neighbors). Finally, under the mate guarding hypothesis, it is unclear why males would pursue EPF rather than guard, since reduced guarding appears to be costly. These issues must be addressed before it is clear whether there is a functional or mechanistic link between breeding synchrony and extrapair fertilization rates.
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ACKNOWLEDGEMENTS |
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This research was conducted in the Hubbard Brook Experimental Forest, which is administered by the USDA Forest Service, Northeastern Research Station, Radnor, Pennsylvania, USA. We thank the numerous field assistants who made this study possible, particularly J. Barg, S. Mauro, and H. Murphy. P. Dunn, H. Lasker, P. Sherman, S. Sillett, D. Taylor, D. Westneat, and two anonymous reviewers provided valuable comments and discussion. Funding was provided by grants from the National Science Foundation (USA) to the State University of New York at Buffalo and to Dartmouth College.
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