Behavioral Ecology
doi:10.1093/beheco/ark002
Advance Access publication 5 May 2006
Genetic evidence for kin-based female
social structure in common eiders
(Somateria mollissima)
Laura McKinnon,a H. Grant Gilchrist,b and Kim T. Scribnera,c
Department of Zoology, Michigan State University, 13 Natural Resources Building, East Lansing, MI
48824-1222, USA, bCanadian Wildlife Service, National Wildlife Research Centre, Carleton University,
1125 Colonel By Drive, Raven Road, Ottawa, ON K1A 0H3, Canada, and cDepartment of Fisheries and
Wildlife, Michigan State University, 13 Natural Resources Building, East Lansing, MI 48824-1222, USA
a
Kin-based social groups are commonly studied among cooperatively breeding species but have been less studied in ‘‘nontraditional’’ group breeding systems. We investigated the presence of kin-based sociality among females in the common eider
(Somateria mollisima), a colonial nesting sea duck that exhibits high levels of natal philopatry in females. Previous studies of
female sociality in common eiders have been restricted to observations during brood rearing. However, aggregations of female
common eiders are also observed during other periods of the life cycle such as colony arrival and nesting. Here we apply a novel,
empirical framework using molecular markers and field sampling to genetically characterize female social groups at several stages
of the common eider life cycle. When compared with mean estimates of interindividual relatedness for the entire colony,
significantly higher levels of relatedness were found between females within groups arriving to the colony in flight, between
females and nearest neighbors at the time of nest site selection, and between groups of females departing the colony with
ducklings. Both full-sibling and half-sibling equivalent relationships were also found within these groups. Therefore, throughout
each of several stages including in-flight colony arrival, nesting, and brood rearing, we provide the first genetically confirmed
evidence of female kin-based social groups in common eiders and anseriformes in general. Key words: common eider, kin groups,
microsatellites, relatedness, sociality. [Behav Ecol 17:614–621 (2006)]
in-based social groups have been described in many species based on both duration of association (ephemeral to
permanent) and composition (sex, age, etc.) (reviewed in
Queller and Strassmann 1998; Griffin and West 2003). In taxa
where kin-based social groups are comprised exclusively of
females, group association may serve to lower the predation
risk of uniparental care while increasing access to resources
for adults (Sterk et al. 1997). For example, female sperm
whales form ‘‘babysitting’’ groups so that some females can
dive to optimal feeding areas without leaving their young unattended and vulnerable to predation (Whitehead 1996). Female primates also form social relationships with female kin,
which decrease predation risk (Sterk et al. 1997) and increase
reproductive success (Pope 2000).
Among birds, social groups have been most extensively
studied in cooperatively breeding species where individuals
forego their own reproduction in order to help other related
members reproduce (Schoech et al. 1996). However, among
some noncooperatively breeding species, female social groups
occur during the brood-rearing period, apparently to decrease predation risk and increase access to resources for
adults (Cooper and Miller 1992; Cezilly et al. 1994; Moreno
et al. 1997). These social groups are often composed of two or
more adult females caring for young from several different
broods (Munro and Bedard 1977a; Eadie et al. 1988; Öst
et al. 2003). This behavior, referred to as brood amalgamation,
is most prevalent in the Anatidae, tribe Mergini (Eadie et al.
K
Address correspondence to L. McKinnon. E-mail: mckinn98@
msu.edu.
Received 1 June 2005; revised 15 March 2006; accepted 30 March
2006.
The Author 2006. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
1988; Boos et al. 1989; Eadie and Lyon 1998; Bustnes et al.
2002). These female social groups typically form during brood
amalgamation and have been most extensively studied in the
common eider (Öst 1999; Öst et al. 2002, 2003, 2005).
Common eiders (Somateria mollisima) are a long-lived, iteroparous species with high adult survivorship, delayed sexual
maturity (Coulson 1984), and strong female philopatry to breeding areas (Cooch 1965; Reed 1975; Wakeley and Mendall
1976; Anderson et al. 1992). Female sociality among common
eiders has been described during brood amalgamation in
common eiders (Öst et al. 2003, 2005). However, common
eider females may form kin-based social groups throughout
several stages of their life cycle, including migration and nesting. Benefits of group cohesion in female common eiders
during colony arrival may include energetic savings during
migration (Alerstam 1990) and the gathering of information
regarding prime nesting areas. Female eiders may also benefit
by nesting in related groups through increased vigilance
against nest predation and intraspecific usurpation (personal
observation). Finally, females with young may benefit by departing with other females if this increased access to resources
and if group vigilance lowered predation.
Kin associations in other Anatidae have been inferred via
behavioral observations or observations of banded individuals
(Elder WH and Elder NL 1949; Regehr et al. 2001; van der
Jeugd et al. 2002), though have rarely been confirmed using
genetic markers (Andersson and Åhlund 2000). The objective
of this study was to identify genetically whether female kinbased social groups exist in common eiders throughout several stages of their life cycle. Given that common eiders are
philopatric to nesting areas, colonial, and exhibit uniparental
care, we predicted that members of aggregations of adult
females during colony arrival, nesting, and colony departure
McKinnon et al.
•
Genetic evidence for kin-based female social structure in Somateria mollissima
615
would be related. Specifically, we predict that estimates of
mean coefficients of relatedness (a surrogate measure of pedigree relationship) between females within groups at all 3
stages would be greater than background levels of relatedness
for females in the colony.
tubes. Blood samples were immediately transferred to a prelabeled centrifuge tube with 1 ml of saline buffer (100 mM Tris,
pH 8.0, 100 mM ethylenediaminetetraacetic acid, 10 mM
NaCl, 0.5% sodium dodecyl sulfate) and stored at ambient
temperature (2–5 C) until transfer to a freezer at the end
of the field season.
METHODS
Colony arrival
To test the hypothesis that aggregations of female common
eiders were composed of related individuals during colony
arrival, mean coefficients of relatedness between females
within arrival groups were compared with the background
levels of relatedness for the colony. Aggregations of females
arriving together were caught in the large mist nets during the
prelaying and early laying period (14 June through 4 July
2003). Females were considered to be arriving in groups if
they entered the net together. Only individuals that were seen
flying together in a cohesive group and were subsequently
captured together were considered arrival groups. This methodology is unique in that it permitted us to capture the natural composition of a distinct group of birds in flight. Blood
was collected from individual females within groups (n ¼ 16
groups) as described above. Blood samples from females captured within groups were used exclusively to estimate mean
relatedness of females arriving together in groups and were
not included in the background levels of relatedness for the
colony discussed above.
Field methods
Study location
Research was conducted at a northern common eider colony
(Somateria mollissima borealis) within the East Bay Migratory
Bird Sanctuary (East Bay) on Southampton Island, Nunavut,
Canada (6402#N, 8147#W) from June to August 2003. The
common eider colony is located on a 26-ha island (Mitivik
Island) within East Bay and consists of up to 4000 breeding
pairs annually. The island is characterized by tundra, low-lying
rocky outcrops, and several ephemeral freshwater ponds. One
larger pond (0.32 ha) exists at the center of the colony and
is a source of freshwater throughout the breeding season.
Wooden study blinds are situated throughout the colony and
are accessed by aboveground canvas tunnels to minimize disturbance to nesting common eiders.
Background levels of female relatedness in the eider colony
To detect female-based kin groups in common eiders in this
study, we tested mean estimates of coefficients of relatedness
among pairs of females within designated groups (arriving
groups, nesting groups, and females departing together in
groups) against the background levels of female relatedness
for the entire colony.
Background levels of female relatedness for this study colony were determined by sampling females on arrival to the
colony. In panmictic populations, the distribution of relatedness values across all pairwise comparisons will be normal with
a mean of zero. In philopatric colonial nesting species, such as
the common eider, higher mean background levels of relatedness between individuals may occur due to natal philopatry
(Coltman et al. 2003). It was therefore necessary to select
a random sample of individuals representative of the population and calculate background levels of female relatedness for
the colony prior to testing for female-based social groups.
Sampling of females was conducted in such a manner as to
fulfill 2 fundamental requirements. First, by selecting a large
number of females (n ¼ 167) coming onto the colony over the
entire arrival period, we captured the genetic diversity of the
entire breeding population. Secondly, we systematically sampled across the entire prelaying and early incubation period
in order to accurately represent the background levels of relatedness for the colony by including early, mid, and late nesters in the sample. A large and temporally representative
sample size helped to ensure that estimates of allele frequencies and estimates of coefficients of relatedness were unbiased. In addition, the background estimate was independent
of the estimates for the 3 sampling groups as females sampled
for the background estimate were not resampled for the other
3 group estimates (colony arrival, nest selection, or colony
departure).
Female common eiders were caught in large nylon salmon
gill nets (6 m tall by 100 m long) erected on the colony during
the prelaying and early laying period (14 June through 4 July
2003). Nets were set in the flight paths of common eiders
flying around the seaward edge of the colony. A maximum
of 2 nets were set simultaneously. At this site, eiders generally
arrive in mixed sex flocks varying in size from 2 to 30 birds.
Approximately 0.25 ml of blood was taken from the tarsal vein
of target female samples using a 25-gauge needle and capillary
Nest site selection
To test the hypothesis that aggregations of female common
eiders were composed of related individuals during nesting,
mean coefficients of relatedness were estimated between focal
females (defined below) and nearest neighbors during nesting, and these were compared with the background levels of
relatedness for the colony. We monitored the location and
timing of nest initiation of female eiders in 2 0.175-ha study
plots. The 2 study plots were located in low-and high-density
nesting areas and were approximately 100 m apart from each
other. Detailed maps were constructed for each monitored
plot, and nest locations were plotted for each female as nests
were initiated over time. Plots were monitored twice daily for
the presence of nesting females from 19 June until 8 August
2003. Nest initiation date was recorded only after a female
had been present on the same nest for at least 3 consecutive
observation periods (approximately 1.5 days) indicating the
initiation of incubation. It is possible that different females
may visit the same nest earlier in the laying period (after the
first or second egg) due to brood parasitism or nest takeover
(Robertson 1998). By recording the initiation date only on
commencement of incubation, when nest takeover is rare
(Robertson 1998), and by sampling feathers at the end of
incubation, it is most likely that the sample reflects the female
who selected to nest in the area and not just a visiting brood
parasite. Initiation dates, presence of attending males and/or
females, hatch dates, and number of ducklings departing the
nest were recorded for each monitored nest. Nesting females
were categorized as early, mid, or late nesters based on the
distribution of nest initiation dates for each plot.
Focal females were randomly selected from each of these
categories using a random number generator. Plot maps were
then used to select the 3 nearest neighbors that were present
prior to nest initiation of each focal female. A nearest neighbor female was defined, based on mapped nest sites, as a
female that was nesting closest to the focal female and was
present in the study plot when the focal female initiated nesting. When approximately 80% of females in the study plots
had departed the nest, nests were visited for collection of
feathers for use in genetic analysis. In cases where nest material
Behavioral Ecology
616
was not available for one or more of the nearest neighbors,
additional females were chosen based on the same criterion
until 3 nearest neighbors were sampled. A total of 13 focal
females, each with 3 nearest neighbors, met this conservative
criterion.
Colony departure
To test the hypothesis that aggregations of adult female common eiders departing the colony with young were composed
of related individuals, mean coefficients of relatedness between females within groups departing together were compared with the background levels of relatedness for the
colony. Females departing the island together in groups were
captured from 24 July through 2 August 2003. Two 8 3 8 3 4–m
wire walk-in traps were constructed and placed on the shore of
the island. As groups departed, they were passively funneled
into the walk-in traps via 50 m lengths of 0.5-m-high chicken
wire fencing that extended at 45 angles from the trap entrances. Traps were checked at 2-h intervals. Both females
and ducklings captured were banded and bled as above.
Groups (n ¼ 11) ranged in size from 2 to 5 females with 3
to 20 ducklings. Parent–offspring relationships were also estimated for females and ducklings within each group to identify
accompanying failed breeders and/or nonbreeders with no
ducklings of their own in the group.
Genetic analysis
DNA was extracted from all blood samples using Qiagen
DNEasy extraction kits (Qiagen, Bothel, WA). DNA was quantified using a spectrophotometer and diluted to 20 ng/ll for
amplification. DNA was extracted from all feather samples in
the same manner. Only 5 contour feathers were used per nest
due to the potential for genetic contamination (i.e., feathers
from different individuals in the same nest). Reducing the
number of feathers selected can reduce the potential for contamination (Pearce et al. 1997). Extracted feather samples
were amplified undiluted due to low concentration of DNA.
DNA was amplified using polymerase chain reaction (PCR)
for 10 microsatellite loci: Sfil5, Alal1(Fields and Scribner
1997), Sfil9, Sfil10, Sfil11 (Libants S, Oswald K, Olle E,
Scribner K, unpublished data), Hhil5, Bcal11 (Buchholz
et al. 1998), Smol4, Smol10 (Paulus and Tiedemann 2003),
and Aphl23 (Maak et al. 2003). All loci were run under published PCR conditions with slight modification (McKinnon
2005). Due to the low concentration of DNA extracted from
the feather samples, feather samples could not be reliably
amplified at 2 of these loci (Sfil11 and Sfil5), so analyses
for the nest site selection study were conducted using only 8
loci. PCR products were run on 6% denaturing acrylamide
gels along with a molecular base pair ladder and standards
of known size. Gels were scanned with a Hitachi FMBIO II
scanner. Alleles were hand scored for each individual. Initial
allele scores were double checked by a second experienced
lab member. Approximately 8–10% of samples, randomly selected from across all groups, were reamplified for each locus
to test for genotyping error due to allelic dropout, contamination, scoring etc. The genotyping error was reported as
the proportion of alleles scored incorrectly, averaged across
all loci.
To obtain background allele frequencies for the populations, a total of 167 individuals were selected systematically
from all females caught in the net (not including those within
arrival groups), representing the entire range of arrival times
for all females. Estimates of allelic frequencies were generated
in the program Microsatellite analyzer, version 3.15 (Dieringer
and Schlotterer 2002). Allelic diversity and observed and
expected heterozygosity were calculated using the program
Genepop, version 3.3 (Raymond and Rousset 1995). Tests for
deviation from Hardy Weinberg equilibrium and tests for linkage disequilibrium between loci (Bonferroni corrected [Rice
1989] to adjust nominal alpha levels for multiple testing)
were also conducted using the program Genepop, version
3.3 (Raymond and Rousset 1995), with exact tests using the
Markov chain method. Pairwise coefficients of relatedness
were calculated using the program Kinship, version 1.3.1
(Goodnight and Queller 1999). Pairwise coefficients of relatedness provide a measure of relatedness between 2 individuals
and are estimated based on the proportion of alleles shared
between individuals adjusted based on population allele frequencies. Standard parametric statistics cannot be used to detect differences in mean estimates of relatedness between
groups due to the interdependence of the pairwise estimates
(Danforth and Freeman-Gallant 1996). Instead, differences in
mean pairwise coefficients of relatedness between groups
were determined via a one-tailed distribution free permutation test with 1000 repetitions. A one-tailed test was chosen
due to the testing of directional hypotheses (i.e., the mean of
the selected group is greater than the background). The permutation test was performed using a SAS-based program. This
program calculates the difference between the means of the
2 groups, then pools the data from both groups, and randomly subsamples 2 new groups from the pooled data. The
difference between the means of the 2 subsampled groups is
calculated for each iteration. The number of times that the
difference in means of the subsampled groups is greater than
the observed difference in means provides a measure of significance, reported as a P value. The permutation test provides a more robust test than alternative nonparametric
statistical tests (Danforth and Freeman-Gallant 1996).
To provide a description of group composition in terms of
relatedness between individuals within groups, we further estimated the likelihood that alleles between individuals were
identical by descent using the program Kinship, version 1.3.1.
(Goodnight and Queller 1999). We tested whether coefficients of relatedness were significantly more likely under the
hypotheses of full-sibling equivalent relationships (rxy ¼ 0.50)
or half-sibling equivalent relationships (rxy ¼ 0.25) than under
the null hypothesis of 2 individuals being unrelated (rxy ¼ 0).
Program Kinship calculates the probability of detecting observed pairs of individuals with multilocus genotypes consistent with these pedigrees conditional on estimated population
allele frequencies. Estimates of statistical significance and
power were calculated by simulating genotypes given the allele frequencies of the population. P values (the probability of
falsely rejecting the null hypothesis) under 0.05 were considered significant. Estimates of statistical power (the probability
of failing to reject a false null hypothesis) were reported as b
(power ¼ 1 b). The calculation of b was based on the
number of loci and estimated heterozygosity for each locus
(Goodnight and Queller 1999).
RESULTS
Genetic analysis
Allelic frequencies, allelic diversity, and observed and expected heterozygosity for each locus were high (Table 1).
The mean number of alleles per locus was 12.4 (standard deviation [SD] ¼ 3.16, range 4 –33) (Table 1). Genotypic frequencies of 8 loci were consistent with Hardy Weinberg
expectations (P . 0.005, Bonferroni corrected), whereas
genotypic frequencies at 2 loci were not (Smol4, P ¼
0.0016, and Hhil5, P ¼ 0.0033). Smol4 was highly polymorphic (33 alleles) (Table 1). The background sample size (n ¼
167) was not large enough to represent the full range of
McKinnon et al.
•
Genetic evidence for kin-based female social structure in Somateria mollissima
617
Table 1
Allelic diversity and observed and expected heterozygosity for
background samples at 10 polymorphic loci
a
b
c
Locus
Het. obs.a
Het. exp.b
Fc
Allelic
diversity
Sfil10
Sfil9
Alal1
Hhil5
Sfil5
Sfil11
Smol10
Aphl23
Smol4
Bcal11
Mean
0.813
0.714
0.652
0.103
0.730
0.462
0.813
0.613
0.850
0.130
0.588
0.855
0.744
0.631
0.122
0.769
0.460
0.801
0.586
0.943
0.130
0.603
0.049
0.040
0.034
0.153
0.052
0.012
0.014
0.046
0.099
0.007
0.026
23
8
6
4
16
6
18
6
33
4
12.4
Observed heterozygosity.
Expected heterozygosity.
Deviation from Hardy Weinberg equilibrium; positive values
indicate heterozygote deficiency and negative values indicate
heterozygote excess.
possible genotypes (531) for such a polymorphic locus, a common problem when estimating population gene frequencies
from samples (Nei 1987). However, Smol4 and Hhil5 were
included in both estimates of coefficients of relatedness and
likelihood tests of pedigrees as the deviation from Hardy
Weinberg expectations was either minimal (Hhil5) and/or
due to small sample size (Smol4) and consequently would
not likely bias estimates. Tests for linkage disequilibrium confirmed that all loci were independently inherited (P . 0.005,
Bonferroni corrected). The genotyping error rate was estimated to be 0.0302 averaged across all loci, well within the
lower range of error rates (0.001–0.127) reported in previous
studies (Hoffman and Amos 2005). Genotype scores were
corrected, and all gels were reviewed again. As an additional
precautionary measure, all homozygotes for several loci were
reamplified to reduce errors due to allelic dropout.
Figure 1
Distribution of relatedness values (A) between females within
arriving groups (n ¼ 16 groups), (B) between females and 3 nearest
neighbors (n ¼ 13 groups), and (C) between females in departing
groups (n ¼ 11 groups) compared with background levels of
relatedness for the colony (n ¼ 167 individuals).
the null hypothesis that female associations present at the
time of colony arrival are random was rejected.
Background levels of female relatedness in the colony
Nest site selection
Background levels of female relatedness (rxy) in this colony
were normally distributed with a mean close to zero (10 loci:
rxy ¼ 0.004, standard error [SE] ¼ 0.002; 8 loci: rxy ¼ 0.006,
SE ¼ 0.002) (Figure 1 and Table 2). A mean rxy of zero for
background random female samples indicates that, on average, females in the colony that were not sampled as part of
identified groups were not related to one another.
We tested the hypothesis that aggregations of female common
eiders were composed of related individuals during nesting.
When focal females initiated nests, there was an average of 32
(SD ¼ 4.8, range 16–83) females nesting in the study plots.
Nearest neighbors initiated nests on average 2.6 (SE ¼ 0.44,
range ¼ 0–13) days before focal females initiated their own
nests. The mean estimate of pairwise relatedness for focal
females and their 3 nearest neighbors (rxy ¼ 0.060, SE ¼
0.046) was significantly greater than the mean background
level of relatedness for the colony (rxy ¼ 0.006, SE ¼
0.002; permutation test, P ¼ 0.012; Table 2 and Figure 1B),
indicating that females that were spatially aggregated during
nesting were related to each other. Two focal females had 2
full-sibling equivalent relationships with their nearest 3 neighbors (P , 0.05, b ¼ 0.101). Another 3 focal females had one
full-sibling equivalent relationship within the nearest 3 neighbors (P , 0.05, b ¼ 0.101). An additional 2 focal females had
half-sibling equivalent relationships (rxy ¼ 0.25) within the
nearest 3 neighbors (P , 0.05, b ¼ 0.481). Thus, a total of 7
of 13 focal females had at least half-sibling equivalent relationships within the 3 nearest neighbors. The null hypothesis that
female associations during nest site selection are random was
rejected.
Colony arrival
We tested the hypothesis that aggregations of female common
eiders were composed of related individuals during colony
arrival in flight. The mean estimate of pairwise relatedness
for females within arriving groups (rxy ¼ 0.069, SE ¼ 0.036)
was significantly greater than was estimated for the mean
background level of relatedness for the colony (rxy ¼
0.004, SE ¼ 0.002; permutation test, P ¼ 0.034; Table 2
and Figure 1A), indicating that aggregations of females during colony arrival were composed of some related individuals.
Estimates of relatedness consistent with full-sibling equivalent
relationships (rxy ¼ 0.50) were present in 4 of 16 arrival groups
(P , 0.05, b ¼ 0.044). Included in these groups was one group
of 4 females with 3 full-sibling equivalent relationships. Thus,
Behavioral Ecology
618
Table 2
Mean pairwise relatedness values as calculated in Kinship 1.3.1 (Goodnight and Queller 1999) for all
groups and results of one-tailed permutation tests testing for differences between mean relatedness of
females in groups versus background levels
Group
Sample size
Mean pairwise
relatedness values
Background (10 loci)
Arrival groups
Background (8 loci)
Focal females and 3 nearest neighbors
Background (10 loci)
Departing groups
167 individuals
16 groups
167 individuals
13 groups
167 individuals
11 groups
0.004
0.069
0.006
0.060
0.004
0.055
(0.002)
(0.036)
(0.002)
(0.046)
(0.002)
(0.033)
Permutation test
(P value)
0.012
0.039
0.047
SEs of the means are reported in parentheses.
Colony departure
We tested the hypothesis that aggregations of adult female
common eiders departing the colony with young were composed of related individuals. Mean departing group size was
11.33 (SD ¼ 5.80, range 5–23). The average number of adult
females per departing group was 2.40 (SD ¼ 1.24, range 1–5),
the average number of ducklings was 8.93 (SD ¼ 1.28, range
4–20), and the average ratio of ducklings to adult females in
captured groups was 3.72:1. The mean estimate of pairwise
relatedness for adult females within departing groups (rxy ¼
0.055, SE ¼ 0.033) was significantly greater than the mean
background level of relatedness for the colony (rxy ¼
0.004, SE ¼ 0.002; permutation test, P ¼ 0.047; Table 2
and Figure 1C), indicating that aggregations of females during colony departure were composed of related individuals.
Each departing group had one female that did not have
parent–offspring equivalent relationships with any of the
ducklings in the brood. Full-sibling equivalent relationships
were found between females in 2 departing groups. One departing group included 2 full-sibling equivalent relationships
(P , 0.05, b ¼ 0.052) and a second departing group had 1
full-sibling equivalent relationship (P , 0.01, b ¼ 0.163)
between adult females. Thus, the null hypothesis that female
associations present at the time of colony departure are random was rejected.
DISCUSSION
Based on genetic evidence, we found that kin groups occurred
during colony arrival, nest site selection, and colony departure
and, therefore, we reject the null hypothesis that social groups
in common eider females are random with respect to relatedness. When compared with the mean estimates of interindividual relatedness for the entire colony, significantly higher
levels of relatedness were found between females within
groups arriving to the colony in flight, between females and
nearest neighbors at the time of nest site selection, and between groups of females departing the colony with ducklings.
Collectively, results provide evidence for kin-mediated sociality in common eider females.
Colony arrival
Confirmation of female kin groups arriving in flight together
at the breeding colony provides the first direct evidence for
female–female bonds documented in sea ducks during flight.
The presence of full-sibling equivalent relationships within
these groups suggests that offspring may follow the females
and/or siblings from hatch, beyond the brood-rearing period,
throughout the fall molt and migration to wintering areas,
and during their return to the colony. This has not been previously observed in tribe Mergini. Evidence of extended kin
groups (young with adults) has been suggested for another
sea duck, the harlequin duck (Histrionicus histrionicus; Cooke
et al. 2000; Regehr et al. 2001), and geese (Elder WH and
Elder 1949) based on sightings of juveniles arriving with
adults on the wintering areas. These suggested relationships,
however, have not previously been confirmed genetically.
Detection of half-sibling equivalent relationships may also
indicate that family groups can persist across several years or
across extended family members. An rxy value of 0.25 can be
explained through a variety of mechanisms including, but not
limited to, an offspring following other female relatives,
young from multiple years following a mother, or half-siblings
from a multiply sired clutch (e.g., Hario et al. 2002). Prolonged (.2 years) mother–offspring and sibling relationships
have not been commonly observed in anseriformes (Black
and Owen 1989; review in Raveling 1979; Owen 1980; Prevett
and MacInnes 1980). Though patterns of prolonged parent–
offspring bonds and extended family units have been documented in migrating geese (Ely 1993; Warren et al. 1993) and
swans (Scott 1980), studies were based on behavioral observations or visual observations of banded individuals and lacked
genetic confirmation of mother–offspring and sibling relationships. The presence of prolonged or extended bonds
within migrating groups can increase the potential fitness
benefits of group travel as younger individuals may benefit
from the experience of older group members. Here, we present the first genetic evidence of mother–offspring or sibling
equivalent bonds during colony arrival and possibly migration
and the first genetic evidence of potential prolonged or extended family relationships for common eiders specifically
and among anseriformes in general.
It is possible that the females captured in arrival groups
could have already been in the colony, selected a nesting area
and left to forage with females from that same area, and were
captured on return to the colony. Relationships within these
groups may then be explained by the clustering of kin during
nesting at the colony (discussed in detail below) and not by
clustering of kin prior to arrival at the colony. Thus, females in
arrival groups could represent migrating individuals or simply
individuals foraging together. Regardless, the elevated levels
of relatedness within the arrival groups do indicate some form
of in-flight kin-based group cohesion, which could be present
during migration.
Nest site selection
Spatial clustering of kin during nesting has been documented
in many species by identifying general spatial patterns of relatedness in breeding areas (i.e., correlation of relatedness
McKinnon et al.
•
Genetic evidence for kin-based female social structure in Somateria mollissima
and geographic proximity) (e.g., Friesen et al. 1996; Burland
et al. 2001; Ratnayeke et al. 2002; van der Jeugd et al. 2002).
Fewer studies actually examine the decision-making process
during nest site selection by individual animals (Andersson
and Åhlund 2000). Female common eiders investigate several
nest sites, often sitting in them, before choosing the final nest
cup (Cooch 1965; Schmutz et al. 1982; Bottita et al. 2003). By
examining the levels of relatedness between focal females and
their nearest neighbors at the time of nest site selection, we
have confirmed a preference for nesting in proximity to kin.
Given the abundance of females nesting in these areas when
focal females selected nests and the high prevalence of fulland half-sibling equivalent relationships between focal females and their 3 nearest neighbors, these results suggest that
kinship is a factor in nest site selection.
Given evidence of kin groups in arriving females, it is not
surprising to find higher levels of relatedness between nesting
females and their nearest neighbors. If females were arriving
together, it is possible that they may be selecting nest sites at
the same time, in the same locations based on other ecological factors such as proximity to water, distance to the nests of
predators, and characteristics of available nest cups themselves (Kilpi and Lindström 1997). Females arriving together
may nest together in the highest quality areas available at the
time of arrival. However, the nearest neighbors selected in
this study initiated nests, on average, 2.6 days earlier than the
focal females, clearly indicating separate nest initiation times.
In addition, females arriving together in groups can vary in
breeding condition. For example, of females caught in the net
at the same time, some laid an egg while in the holding box
within an hour of capture, whereas others prospected for nesting areas for several days before finally selecting a nest site and
laying. This suggests that although individuals may arrive together, nesting among arriving individuals is not necessarily
synchronous, and therefore it is unlikely that these patterns
are solely an artifact of similar colony arrival times. It is more
likely that there is some level of kin recognition among female
common eiders, similar to that suggested for goldeneye ducks
during brood parasitism, where females preferentially parasitize the nests of close relatives (Andersson and Åhlund 2000).
Female philopatry might also account for higher levels of
relatedness between nearest neighbors. Common eiders are
often philopatric to nesting areas within colonies (Cooch
1965), and fidelity to specific nest sites, though rare, has been
documented (Goudie et al. 2000). Natal philopatry could explain close proximity of kin in nesting areas regardless of nest
site selection processes. Studies conducted on other seabird
colonies (Osorio-Beristain and Drummond 1993; Friesen et al.
1996; Schjorring 2001) have shown that individuals showed
a greater preference for nesting in proximity to natal nesting
areas as opposed to kin. These species, however, exhibit both
male and female philopatry, and pair bonds form on the
breeding grounds. Nesting in close proximity to kin could
be detrimental in species where both sexes are highly philopatric and breeding colonies are small in number due to
increased risk of inbreeding (Shields 1982, 1987). In northern
common eiders, only females are philopatric, and pair bonds
are thought to form on the wintering grounds. Consequently,
in common eiders, the process of selecting nests in close
proximity to kin should not lead to the negative consequences
of inbreeding. Based on the data presented here, it is more
likely that there is a nest site selection process that involves kin
recognition. Though the mechanisms of kin recognition remain poorly understood in birds (Komdeur and Hatchwell
1999), several studies in philopatric species have documented
a preference for nesting in proximity to kin even when nesting
away from natal breeding sites (Andersson and Åhlund 2000;
van der Jeugd et al. 2002).
619
Colony departure
Relatively higher levels of relatedness between females in departing groups could be a result of arrival in kin groups, nesting in kin groups, or a combination of both. If females are
arriving together, they may be nesting at the same time, and
consequently clutches would hatch synchronously and females would depart with young at the same time. It is likely
then, if brood amalgamation is to occur, that females in departing groups may be relatively closely related to each other
due to their timing of arrival and nesting associations (discussed above). One proposal, the accidental mixing hypothesis (Munro and Bedard 1977b; Warhurst and Bookhout 1983;
Eadie et al. 1988), partially explains this phenomenon in
breeding females, where there is a propensity for broods to
amalgamate accidentally due to high brood density (Patterson
et al. 1982; Warhurst and Bookhout 1983; Savard et al. 1989)
and/or during the confusion of a predation attack (Munro
and Bedard 1977b). Associations of adult females that amalgamate broods could be random due to accidental mixing of
young, but patterns of relatedness would still exist due to
higher relatedness between females that arrived together in
the same breeding condition and thus were departing the
island at the same time. However, not all female associations
during colony departure occur as a result of the accidental
mixing of broods. Females with no young of their own also
accompany departing groups. Recent satellite telemetry data
from our field site indicate that many nonbreeders or failed
breeders remain within 10 km of the colony, feeding in the
bay, throughout the breeding season (HG Gilchrist, unpublished data). These females routinely return to the colony
during late incubation periods and attend incubating females
(Munro and Bedard 1977a; Schmutz et al., 1982; HG Gilchrist,
unpublished data). Nonbreeders or failed breeders will often
attend incubating females at the nest just prior to hatch (usually 24 h prior) (Munro and Bedard 1977a; Schmutz et al.
1983; Bustnes and Erikstad 1991) and subsequently escort
the brood from the nest site to the marine habitats.
The presence of failed breeders or nonbreeders in departing groups might be explained by female nest site selection,
prolonged female offspring or sibling bonds, female philopatry to natal nesting areas, or combinations of these. For example, when nesting attempts fail, female eiders often depart the
breeding area to recover nutritional reserves (Gorman and
Milne 1972) but may return to attend broods in the same area
of their failed nesting attempt as opposed to a different area
in the colony. The adaptiveness of attending departing groups
with relatives for a failed or nonbreeder could be explained by
kin selection if duckling survival was enhanced by this attendance. Campbell (1975) presents evidence suggesting that the
time period between hatching and departure from the nest
(24 h), not the departure itself, is the period of greatest predation risk for ducklings (Campbell 1975). At the East Bay
eider colony, attending females, on average, tend to arrive at
the nests of incubating females 1.86 days before departure,
precisely during this critical hatching period. Their presence
at the nest may decrease predation pressure because we have
observed attending females defending eider nests against herring gull attacks. However, we recognize that despite evidence
of vigilant behavior by failed breeders or nonbreeders during
predation attacks on ducklings (Schmutz et al. 1982), increases in duckling survival due to these attending females
remain unconfirmed (Ahlen and Andersson 1970; Campbell
1975).
The size, degree of isolation, and spatial contiguity of nesting habitat characterizing breeding colonies may also affect
the extent to which philopatry can influence the kin composition of departing female groups. On relatively large, isolated
Behavioral Ecology
620
breeding colonies such as our site, breeding habitat is contiguous and philopatry is often strong (Baillie and Milne 1989;
Bustnes and Erikstad 1993) and may be maintained via isolation. However, common eider females may also nest in colonies on archipelagos or other disjunct habitats where
breeding sites are widely dispersed (Goudie et al. 2000) and
where the composition (social or familial) of contiguously
nesting groups that are available to form coalitions may vary.
Öst et al. (2005) collected genetic data on 24 coalitions of
female common eiders from 18 nesting islands in an archipelago in the Baltic sea and concluded that common eider females formed brood-rearing coalitions composed of unrelated
individuals. Despite high levels of female philopatry in the
archipelago, Öst et al. (2005) noted that the spatial dispersion
of nesting females across many small islands may have affected
the kin composition of coalitions.
Intense social interactions between common eider females
begin during the first few days after hatch (Öst and Kilpi 2000).
By capturing females and ducklings in broods during departure from the island itself and prior to the formation of stable
creches (as studied in Ost et al. 2005), we have generated the
first genetic information confirming kin relationships between
females early in coalition formation. Although there was the
potential for biases in composition of groups captured due to
the nature of the walk-in traps and the varying cohesiveness of
departing groups, the ratio of ducklings to females in captured
broods (3.72:1) was consistent with those recorded for naturally occurring departing broods in other studies (3.5:1,
Gorman and Milne 1972; 2.1–3.1:1, Swennen 1989; 5:1, Öst 1999).
CONCLUSIONS
Throughout each of several stages, colony arrival, nesting, and
brood rearing, we have provided evidence of sociality and
kin groups among common eiders. Though we have not measured direct or indirect associated fitness benefits, previous
avian studies have indicated possible fitness benefits of sociality and kin groups during migration (Alerstam 1990), nesting
(van der Jeugd et al. 2002), and brood amalgamation (Munro
and Bedard 1977b; Öst et al. 2002). Benefits of prolonged
female bonds in common eiders might include an increase
in individual adult survival due to increased group size. For
example, larger group size on the wintering grounds could
increase survival via thermoregulatory benefits during roosting (Gilchrist and Robertson 2000) and/or by lowering predation risk by vigilance and dilution effects. However, indirect
benefits may be reduced via increased competition between
relatives (Griffin and West 2002).
Here we provide genetic evidence for kin-based female social structure in common eiders throughout the breeding season. Though the selective consequences of these social groups
are still unknown, the genetic data presented here suggest
that kin selection is a potential hypothesis to test the adaptiveness of these social behaviors in the common eider. Further
research directed at measuring fitness benefits of sociality in
common eiders and other anseriformes could provide important insight into the benefits and evolution of sociality among
these species.
Funding for this project was provided by the Department of Zoology
and the Department of Fisheries and Wildlife at Michigan State University and grants from the Dr Marvin Hensley Foundation and the
George and Martha Wallace Foundation through Michigan State
University. Fieldwork was funded by the Canadian Wildlife Service,
Environment Canada. Additional logistical support was provided by
Polar Continental Shelf Project (Natural Resources Canada) and the
Nunavut Research Institute. We thank all those who participated in
fieldwork especially H. Jewell, D. McCruer, C. Fournier, K. McKay,
J. Bety, C. Anderson, P. Fast, M. Fast, and K. Allard. Invaluable laboratory assistance was provided by S. Libants, K. Filcek, L.Garzel,
B. Williams, and J. McGuire. We also thank C. Lindell, H. Prince,
and K. Holekamp for their comments on the manuscript. Special
thanks to the Hunter’s and Trapper’s Association and community
members of Coral Harbour, Nunavut, for supporting the research conducted at the East Bay Migratory Sanctuary, specifically Joe Nakoolak
for the essential transportation to Coral Harbour.
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