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Behavioral Ecology Vol. 12 No. 5: 640-645
© 2001 International Society for Behavioral Ecology
Fitness consequences of long-term pair bonds in barnacle geese: monogamy in the extreme
Department of Wildlife, Humboldt State University, Arcata, CA 95521, USA; Department of Arctic Ecology, Norwegian Institute for Nature Research, The Polar Environmental Centre, N-9296 Tromsø, Norway; and The Wildfowl & Wetlands Trust, Slimbridge, Gloucestershire GL2 7BT, UK
Address correspondence to J.M. Black at Humboldt State University. E-mail: jmb7002{at}humboldt.edu .
Received 24 March 2000; revised 2 January 2001; accepted 24 January 2001.
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ABSTRACT |
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In barnacle geese Branta leucopsis, pair-bond members generally remain together every day, each year, often for life. Geese that maintain long-lasting pair bonds during their lifetime produce more offspring than those with shorter pair durations. This result was shown while statistically controlling for the birds' life span and the proportion of life spent without a partner, two variables that also influence lifetime reproductive success. I argue that continuous partnerships are maintained in highly competitive goose societies because of the constant need for female—male cooperation, without which acquiring adequate resources for reproduction would be prohibitive for both sexes.
Key words: barnacle geese, Branta leucopsis, cooperation, monogamy, lifetime reproductive success, mate familiarity, mate fidelity, pair bonds, partnerships, site fidelity.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Perennial monogamy, defined as the annual reestablishment or continuous maintenance of pair bonds, occurs in a variety of animals. This extreme form of social monogamy is common in birds, occurring in at least 50% of the 28 orders and 21% of the 159 avian families (Black, 1996
). Describing the
adaptive significance of long-term pair bonds is a difficult task because it
requires researchers to track the social status and fate of individuals over
entire lifetimes.
In 8 of 15 long-term studies, there was a clear relationship between annual
reproductive success (ARS) and the length of time pair members were together
(Ens et al., 1996). This was
most apparent in long-lived species with continuous partnerships—6 of
the 8 species maintaining contact throughout the annual cycle
(Ens et al., 1996). In geese
and swans, for example, ARS increased for the first 6-11 years of the
partnership (Black et al.,
1996; Rees et al.,
1996). It was suggested that ARS is enhanced as pair members'
behavioral repertoire is fine-tuned, thus coordinating efforts and acquiring
more essential resources (referred to as the "mate familiarity
effect"; Black, 1996).
Potential behaviors involved may include participation in sentinel behavior,
competition for foraging space and nest sites, and defense against
predators.
However, before a more solid claim can be made that maintaining pair bonds
is adaptive in these bird populations, several alternative explanations for
the results must be considered. Ens et al.
(1996) pointed out that
longitudinal analyses of this kind are problematic because ARS may be skewed
by temporal or spatial environmental variation and individuals of different
ages and qualities (often measured by life span) may contribute more than one
ARS and pair duration class value during their lifetimes.
The aim of this study was to reassess the relationship between pair bond
duration and reproductive success while addressing some of the weaknesses of
earlier studies (Black, 1996)
using a long-term data set on barnacle goose Branta leucopsis
partnerships. I deal with the weaknesses by limiting the analysis to one group
of birds living at the same place at the same time (thus removing variation
due to temporal and spatial environmental variation in reproductive success)
and by using a single measure rather than multiple measures of reproductive
success per individual (i.e., lifetime reproductive success, LRS). Barnacle
goose LRS increases with life span (Owen
and Black, 1989a), and the timing of finding a replacement mate
after death of a partner influences the probability of breeding the next
summer (Owen et al., 1988).
Therefore, I simultaneously considered several key variables (e.g., life span,
time without a partner, etc.) while testing the importance of pair-bond
duration on LRS.
Barnacle geese are highly gregarious, living in large flocks and colonies.
Like other arctic geese, barnacle geese store fat and nutrient reserves to
transport to the breeding grounds, where females invest 40-60% of their body
mass during reproductive attempts (Owen,
1980). Those geese that gain access to rich feeding areas are best
able to obtain enough food (Black et al.,
1992; Prop and Loonen,
1988; Teunissen et al.,
1985). A key feature in describing the social system in goose
flocks is the dominance relationship among social groups and their access to
feeding areas (Black & Owen,
1989a,b;
Boyd, 1953;
Lamprecht, 1986a;
Raveling, 1970).
When a single bird establishes a pair bond in its first or second year, it
rises in social rank, matching that of the majority of conspecifics
(Black and Owen, 1987); the
predominant social class in winter flocks is pairs without offspring, which
accounts for 70-99% of the adult population
(Pettifor et al., 1998).
Establishing a pair bond is a prerequisite for acquiring and defending a
nesting territory (see Lamprecht,
1987; Martin et al.,
1985). Pairs that succeed in reproduction and associate with
offspring in family units rise further in social rank above the pairs without
young which predominate in the nonbreeding season; on average, the goslings of
only about 15% of potential breeding pairs survive to 4 months
(Pettifor et al., 1998).
Once the pair bond is established, pair members usually maintain close
proximity (<2 m) and rarely allow nonfamily members to come near
(Black and Owen, 1988;
Siriwardena and Black, 1999).
Most geese have only one mate in their lifetimes
(Black et al., 1996;
Owen et al., 1988), although
many have the opportunity to re-pair after the death of initial partners.
Still fewer geese divorce and re-pair with alternative partners (2% annually),
though this phenomenon is greatest in years when potentially higher quality
partners are available (Black et al.,
1996). Ens et al.
(1993,
1996) suggested that improving
on initial mate choices when a better quality mate is available should result
in a higher reproductive payoff. Contrary to predictions from the mate
familiarity hypothesis, achieving better options may result in a greater
reproductive payoff for individuals having multiple mates in a lifetime. I
tested whether LRS is enhanced in birds with a larger number of mates after
controlling for confounding variables. I discuss the merits of long-term pair
bonds in terms of LRS, offering an explanation for how perennial monogamy may
have evolved and is maintained in arctic geese.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The 119 birds used in this analysis, with known pair bond and LRS information, were drawn from a long-term study in which about 9000 geese were fitted with individually engraved tarsal bands during rocket net catches and molt roundups (Owen, 1987
).
Birds were also fitted with a more permanent metal tarsal-band and sexed by
cloacal examination (Owen,
1980). Bands were routinely identified up to 250 m away during the
birds' 9-month nonbreeding season and periodically during the breeding season
(see Black and Owen, 1995).
Most birds were seen an average of 8 times per year, and about 95% of all
bands were resighted at least once per year, such that there was a 0.14%
chance of missing a bird in 2 consecutive years
(Owen, 1982;
Owen and Black, 1989b).
Movements to other populations were negligible (Owen and Black,
1989a,b).
The end of each life span was therefore determined when a bird was
consecutively missing from the data set for more than 2 years.
On resighting a bird's band-code, an attempt was made to identify the mate
and count the number of goslings in the family unit (Black and Owen,
1989a,b).
Gosling plumage in this species is distinguishable throughout the winter
(Owen, 1980). Within the
flock, family members walk a similar pathway and coordinate vigilance bouts,
aggressive encounters with neighbors, and social displays
(Black et al., 1996). Pairbond
durations were taken from the first to the last date banded partners were
recorded together. I calculated mean pairbond duration for birds with more
than one banded partner. The gaps between partners (when mate information was
recorded as unpaired, alone, or consistently with no mate information) was
summed to determine the amount of time a bird was unpaired in its lifetime. In
some cases, I extended the duration of pair bonds by checking the data set for
consistent associations (i.e., no data indicating an unpaired gap) with an
unbanded bird immediately before capture events (n = 12 cases), or a
metal-only banded bird subsequent to a catch (n = 2 cases). In the
first situation, I assumed that an unbanded partner was recently captured and
banded, and in the second situation that a banded partner had lost its plastic
band.
I calculated LRS as the cumulative number of offspring that associated with
parents on arrival to the wintering grounds (Owen and Black,
1989a,b).
Determination of ARS values was limited to records taken before 1 January each
year because family group cohesion diminishes once goslings reach 6 months of
age, when parents begin behaving aggressively toward their goslings
(Black and Owen, 1989a). When
birds were recorded for the first time after this date without offspring,
their ARS for that year was recorded as "not enough information."
A complete set of ARS information was required for birds living for <10
years. To reduce bias against longer lived birds, I included them when ARS
information was known for at least 90% of the lifetime. With this criteria, an
additional 17 birds living for 10+ years with 1 missing year, and 8 birds
living for 20+ years with 2 missing years were included. I assumed that no
offspring were produced in those missing years because family units are
generally conspicuous in winter flocks (also see
Owen and Black, 1989a).
To avoid including pair-bond durations twice (once for females and again for their mates), I excluded 31 male records when the males' partner(s) were already in the data set. This resulted in fewer male records (28 males, 91 females). Because there was no difference in life history and pair-bond statistics, I pooled the data set.
Statistical approach
To remove variation in ARS due to temporal and spatial environmental
variation, I limited the analysis to the 1976 cohort. These birds were
captured and aged as yearlings on the
Nordenskiöld coast, West Spitsbergen, Norway, in
July—August 1977 (Owen et al.,
1978). I suspect that most birds hatched at this site, though it
is possible that some birds moved there to molt in their second summer.
Especially during the beginning of the study, little movement between colonies
occurred (Black, 1998;
Owen et al., 1988). The few
birds from this cohort that did move to another breeding area were not
included in the analysis.
My prediction, based on the mate familiarity effect hypothesis
(Black, 1996), was that
individuals that remain with a single partner would produce more offspring
than those with more than one mate over the same period. To test whether time
spent with particular partners influenced LRS, I first controlled for
confounding variables using a multivariate SAS Procedure GLM
(SAS Institute, 1996).
Statistical values refer to the final model (partial Type III SS) of a
stepwise procedure. Independent variables (life span, years of life unpaired,
time to first partner, mean pair-bond duration) were treated as class
variables. By including life span, I attempted to control for some of the
variation caused by individual bird quality, in the sense that high-quality
individuals breed consistently and live longer (sensu
Coulson and Thomas, 1985).
A similar GLM analysis was conducted on the effect of pair duration on life expectancy. My prediction, based on the mate familiarity effect hypothesis, concerning likelihood of future survival was that geese that had been with a mate longer (within each age class) would live longer (life expectancy). The analysis was limited to first partnerships and was performed with each age class that contained at least 15 birds. Repeating the analysis for each age class meant that individuals contributed only one record per analysis. There were sufficient data for 16 analyses of bird ages 2-18 years with pair durations ranging from 0 to 17 years. Pair duration was treated as a class variable.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The time it took to establish initial pair bonds ranged between 1 and 5 years, thus delaying the possibility of successful breeding for a substantial part of their lifetimes for some birds (mean age of first pairing = 2.44 ± 0.05 [SE] years). Therefore, the variable time to first partner was significant in explaining LRS (F = 2.97, df = 4, p =.0234) in a preliminary analysis when the primary variable in the model was longevity (F = 5.05, df = 19, p =.0001). Time to first partner became insignificant (F = 0.60, df = 4, p =.6664) and was dropped from the model when time unpaired was added. Time unpaired, the variable used in the final model, includes not only the initial unpaired time before the first mate, but also the time between subsequent mates. The average time unpaired amounted to 33% (SE 1.01%) of the birds' lifetimes. Forty percent of geese had more than one mate during their lifetimes (range 1-4 mates; mean 1.60 ± 0.08). After controlling for life span, the number of mates a bird had in a lifetime did not influence LRS and was therefore not included in the final model (Table 1). There was no difference in LRS for birds paired with just one mate compared with those with more than one mate in a lifetime (Table 1).
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The average duration of pair bonds was 4.70 years (SE 0.37 years), though 17 birds were together for more than 10 years, and 3 were together for 19 years (mean pair duration range = 0.58-19.29 years). After controlling for life span (range 2-21 years, mean 9.26 ± 0.46) and time unpaired (range 1-7 years, mean = 3.52 ± 0.13), mean pair duration significantly affected LRS (Table 1, Figure 1). The order of importance of these variables in the final model was life span, mean pair duration, time unpaired, and an interaction between mean pair duration and time unpaired.
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Life expectancy was not influenced by duration with a partner in barnacle geese in any of the 16 age-class analyses (range of values, F = 0.34-1.59, df = 1-11, p =.3187-.9308). Sample sizes in these analyses ranged from 16 to 108 birds (mean 54.50 ± 8.34).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The results of this study support the earlier proposal that longterm pair bonds are adaptive in this barnacle goose population. In the previous analysis, we found that annual rates of reproduction increased dramatically during the first 6 years that mates were together, before leveling off and declining in the later years (Black et al., 1996
). The use of ARS was potentially problematic in that
analysis, making it difficult to interpret the quadratic pattern of
reproductive success with pair duration
(Ens et al., 1996). New
findings from this study are that the single, more robust measure of fitness,
LRS, is clearly influenced by the length of time pair bonds were established.
This result was achieved while statistically controlling for the birds' life
span (a potential covariate) and time unpaired, two critical features
explaining LRS in long-lived birds. In addition, I limited analyses to a
single cohort from one location, therefore removing the temporal and spatial
environmental bias in reproduction (e.g., Owen and Black,
1989b,
1991).
The portion of a lifetime without a partner was also influential in
explaining variation in LRS in barnacle geese, supporting the idea that an
established pair bond is a prerequisite to reproduction. The variable time
unpaired encompasses the majority of nonbreeding time in geese because it
includes time before the first and between subsequent partnerships. On
average, barnacle geese spent 30% of their lifetimes without a partner. They
generally initiate the first pair bond in the first 24 months of life, and it
takes 3-9 months to replace a mate (Owen
et al., 1988).
If geese chose a better quality mate each time they had the opportunity to
do so (referred to as the "better option hypothesis"; Ens et al.,
1993,
1996), I would expect a higher
LRS for those with more mates in a lifetime. However, I found no indication
that the number of mates in a lifetime affected LRS. Controlling for life
span, birds that had one mate were just as successful as those with two or
more mates. The length of time with particular mates was apparently more
important than the number of mates in a lifetime. Further investigations,
including a comparison between initial and subsequent mate qualities, are
required to substantiate predictions from the better option hypothesis (Ens et
al., 1993,
1996).
Long-term pair bonds may be selected for in goose societies because of the
constant need for female-male cooperation. Male assistance is apparently
essential for females to acquire enough fat and nutrient reserves to enable
breeding attempts (see Lamprecht,
1989). Males act as sentinels and fend off competitors while
females spend most of their time feeding (Black and Owen,
1988,
1989b;
Boyd, 1953;
Forslund, 1993;
Raveling, 1970;
Sedinger and Raveling, 1990).
The pair act together, fighting for and maintaining a territory within the
colony (Collias and Jahn,
1959; Inglis,
1977; Lamprecht,
1987). In barnacle geese, males stand guard and defend eggs from
patrolling gulls while females take short incubation breaks away from nesting
territories (Prop et al.,
1984). During brood rearing, males are the primary defenders of
space in flocks, but females often participate in vigilance routines and
aggressive encounters (Black and Owen,
1989a,b;
Sedinger and Raveling, 1990;
Siriwardena and Black,
1999).
Because prolonged cooperation in pair bonds apparently results in a higher LRS, why does it not also result in greater survival of pair members? The answer is probably linked to the cost of reproduction. In a parallel analysis of life-history tactics, we found that geese producing the most offspring do so early in life, whereas those that postpone reproduction live longer (Black and Erikstad, unpublished data). The costs are not immediately realized, but accumulate, resulting in a shorter life span. Therefore, pair members that coordinate and fine-tune their behaviors may obtain adequate resources for successful reproduction, but at the expense of a long life.
I propose that the mechanism behind enhanced LRS in pairs with long-lasting
partnerships (controlling for life span and time without a partner) is the
social feedback loop, alluded to for geese by Raveling
(1981) and further developed
by Lamprecht (1986b,
1990) and Black and Owen
(1989a,b).
To expand on this idea here, I stress that the usefulness of mate fidelity in
goose societies is linked with their high degree of site fidelity to foraging
and breeding sites. Adult barnacle geese return to the same sites at the
following rates: wintering sites (99%), breeding sites (95%), and staging
sites (90%) (Black, 1998;
Black et al., 1991). At each of
these locations, geese forage in a series of microhabitats that provide
various energetic payoffs compounded by predation risks. Learning to
capitalize on the subtleties of each foraging site may take years
(Black, 1998; Prop and Black,
unpublished data). Choosing a mate that has experience with particular sites
may be advantageous because of enhanced predator awareness, food finding, and
competitive ability.
The social feedback loop is linked to the development of social rank
(dominance) that exists in goose flocks
(Black and Owen, 1987;
Boyd, 1953). For a pair of
geese to succeed in reproduction for the first time, it must compete among the
many other previously unsuccessful birds and the few consistently successful
birds (Owen and Black, 1989a;
Raveling, 1981). Pairs showing
high rates of aggressiveness in the winter flocks are most likely to succeed
the next summer (Black and Owen,
1989b; Lamprecht,
1986b). Once successful, they join other families in brood-rearing
areas, where they proceed to molt flight feathers. On return to the wintering
grounds, families defend foraging space within the outer edge of flocks where
the best food is obtained (Black and Owen,
1989b, Black et al.,
1992). Parental burdens may be reduced by associating with grown
goslings that assist in encounters with neighbors and with vigilance for
competitors and predators (i.e., gosling helper effect;
Black and Owen, 1989a). Parents
and offspring enjoy these and other foraging-related benefits of high social
status as long as they maintain the family unit.
In contrast, when pairs fail to breed in a particular year, they join other
nonbreeders during the molt. In winter they congregate most closely with other
pairs without young in the center of large flocks
(Black and Owen, 1989b;
Black et al., 1996). It is
suggested from the social feedback hypothesis that within this large
contingent of equally matched pairs without offspring (90% of the population
in most years), the social rank is ordered by the pairs' prior accumulated
reproductive success (number and size of previous family units).
I suspect that individual recognition is an essential feature in this
system. Evidence that geese respond favorably to familiar individuals comes
from a series of studies with captive geese
(Choudhury and Black, 1994;
Cowan, 1973; Lamprecht,
1977,
1984;
Radesater, 1976) and
descriptions of individuals' unique vocalizations (Hausberger et al.,
1991,
1994). In captive goose flocks
periods of stability in the social rank are apparently maintained by
individual recognition among flock members
(Lamprecht, 1986a;
Lorenz, 1966). Therefore, the
integrity of pair bonds and the continued use of sites may enable pair members
to maintain and/or increase their position in local social rank hierarchies,
enabling enhanced acquisition of resources. In such a system, maintaining pair
bonds with familiar partners, and those with local knowledge, would be an
advantage. Unless an old mate is replaced with a partner that is
"known," an individual may drop in the social rank and in the
social feedback loop. Regardless, it may take new pairs months or years to
reestablish a competitively successful behavioral routine. Evidence for this
comes from an initial analysis of pair-bond duration and flock position in
winter flocks. Pairs (without offspring) that were together for the longest
periods were more often found competing with dominant family units in the more
profitable outer edge of the flocks (Black
et al., 1996).
Continuous partnerships are probably most beneficial in systems with
repeated or permanent use of sites, including site-faithful or sedentary
species. The multispecies, independent contrast comparison of mate fidelity
(and divorce) in birds by Ens et al.
(1996) supports the notion of
a strong link between continuous partnerships and repeated use of sites. In
their review of more than 100 different bird populations comprising 76
species, mate fidelity was highest (and divorce lowest) in species that were
resident with continuous partnerships, and mate fidelity was lowest (and
divorce highest) in species that were migratory with part-time partnerships
(pair bonds that reestablished only for the breeding season). There-fore,
especially for species with long-term, continuous pair bonds with a high
degree of site fidelity, a well-established partnership may outweigh the
potential benefits of divorce and starting over again.
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ACKNOWLEDGEMENTS |
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It was Myrfyn Owen's initial guidance and inspiration that enabled the creation of the data set. Funding for the work was largely from The Wildfowl and Wetland Trust, and the Norwegian Polar Institute and the Governor of Svalbard provided logistical support in the Arctic. Funding for the analysis was provided by the Norwegian Institute for Nature Research, Department of Arctic Ecology, The Polar Environmental Centre, Tromsø. I am particularly grateful to Sharmila Choudhury, Carl Mitchell, Dave Patterson, and Paul Shimmings for assistance. I thank Mark Colwell, Eileen Rees, and Krysta Rogers for suggestions on earlier drafts.
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