Behavioral Ecology Vol. 13 No. 6: 786-790
© 2002 International Society for Behavioral Ecology
Kin clustering in barnacle geese: familiarity or phenotype matching?
a Department of Zoology, Edward Grey Institute of Field Ornithology, University of Oxford, Oxford OX1 3PS, UK b Evolutionary Biology Centre, Department of Animal Ecology, Norbyvägen 18D, SE-752 36 Uppsala, Sweden c Department of Evolutionary Ecology, Max-Planck Institute for Limnology, August-Thienemann-Strasse 2, D-24306 Plön, Germany d Gotland University, SE-621 67 Visby, Sweden
Address correspondence to H.P. van der Jeugd, Department of Zoology, Edward Grey Institute of Field Ornithology, University of Oxford, Oxford OX1 3PS, UK. E-mail: henk.vanderjeugd{at}zoo.ox.ac.uk.
Received 21 June 2001; revised 21 February 2002; accepted 24 February 2002.
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ABSTRACT |
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We investigated the settling pattern of barnacle geese Branta leucopsis that returned to breed in their natal colony. Females nested close to their parents and sisters, but settling of males conformed to a random pattern. The apparent preference for breeding close to kin in females could be a by-product of extreme philopatry to the natal nest site. However, sisters also nested close to each other when settling on a different island than the one where their parents bred, pointing at a genuine preference for breeding close to kin. Females only nested close to sisters born in the same year (i.e., sisters that they had been in close contact with). This suggests that the clustering of female kin in barnacle geese does not result from phenotype matching. We did not detect any direct benefits of settling close to birth site or kin, but the analyses lacked power to detect small benefits of proximity to kin given the many other factors that may influence breeding success. Colonially breeding birds share characteristics that are generally believed to promote the evolution of cooperation, yet kin clustering and kin selection have been little studied in this group. Future research should be directed to studying the possible roles of kin clustering and kin selection in the evolution of coloniality.
Key words: barnacle goose, Branta leucopsis, coloniality, cooperation, kin selection, phenotype matching, philopatry.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Optimal dispersal patterns of animals are the result of a trade-off between the costs and benefits associated with dispersal and philopatry (Greenwood, 1980
). One
potential benefit of philopatry arises because of the presence of kin in the
natal area (Hamilton, 1964). A
benefit of settling close to kin is the possibility of receiving help from
related individuals, such as is found in highly social species such as
eusocial insects and cooperatively breeding birds and mammals
(Brown, 1987;
Emlen, 1994;
Lessells et al., 1994;
Stacey and Ligon, 1987), but
there might also be more subtle benefits. For example, the level of aggression
might be lower among kin than among unrelated individuals
(Greenwood et al., 1979;
Waldman, 1988;
Watson et al., 1994). Settling
close to kin can facilitate territory acquisition as for example shown in red
grouse Lagopus lagopus scotticus
(Watson et al., 1994).
Evidence that breeding close to kin can increase breeding success comes
primarily from work on microtine rodents, where close relatives are frequently
neighbors (e.g., Lambin and Yoccoz,
1998; Mappes et al.,
1995; Pusenius et al.,
1998). Increased breeding success for males living near relatives
has also been reported in the western gull Larus occidentalis
(Spear et al., 1998). Settling
close to kin may also result in an increased probability of incestuous
pairings, which can potentially lead to inbreeding depression. The fact that
close inbreeding is rarely observed even in highly philopatric species
suggests that animals have mechanisms to avoid breeding with close kin.
A critical element in the evolution of cooperation and avoidance of
inbreeding is the ability to discriminate between kin and non-kin, most
obviously via recognition. However, at present little is known about
recognition mechanisms (Komdeur and
Hatchwell, 1999). One proposed mechanism by which animals can
recognize unfamiliar relatives is phenotype matching. Phenotype matching
involves learning the phenotype of familiar relatives, or of oneself
(self-referent phenotype matching), thereby forming a phenotypic template
against which the phenotypes of unfamiliar individuals can be compared
(Komdeur and Hatchwell, 1999;
Lacy and Sherman, 1983;
Mateo and Johnston, 2000). Kin
recognition by phenotype matching requires that phenotypic similarity reliably
reflects genetic relatedness. There is growing evidence that some animals
might be using some form of phenotype matching. For example, mice have been
shown to use MHC odor type to avoid breeding with close relatives
(Hurst et al., 2001;
Smith et al., 1994;
Yamazaki et al., 2000).
Olfactory cues also seem to be used by Arizona tiger salamanders Ambystoma
tigrinum nebulosum (Pfennig et al.,
1994), and rainbow fish Melanotaenia eachamensis seem to
use both visual and chemical cues to detect shoals of related individuals
(Arnold, 2000). Many studies,
however, have found that individuals only recognize familiar kin (for
experimental evidence, see Griffiths and
Magurran, 1999). There is as yet no conclusive evidence for the
occurrence of phenotype matching in birds
(Komdeur and Hatchwell, 1999),
although the recent finding that some lekking birds display close to relatives
(Petrie et al., 1999;
Shorey et al., 2000) suggests
that birds have the ability to reliably identify relatives among unfamiliar
individuals.
A problem when investigating whether individuals are actively settling
close to kin in highly philopatric species is to exclude the possibility that
they are philopatric because of benefits of settling in the natal area, rather
than because of benefits of settling close to kin. For example,
Schjørring (2001) was
able to show that the clustering of kin within a colony of great cormorants
Phalacrocorax carbo sinensis was due to attraction to the natal nest
site rather than due to attraction to close kin. The study of dispersal of
relatives in colonially breeding seabirds and waterfowl is of particular
interest in this context because virtually all species in this group share
characteristics that are generally believed to promote the evolution of
cooperation, such as long life span, strong philopatry, and limited access to
nest sites (Arnold and Owens,
1998; Hatchwell and Komdeur,
2000; Kokko and Lundberg,
2001). Nonrandom dispersal within colonies of seabirds and
waterfowl has been reported but is usually explained by philopatry to the
natal nest site rather than by attraction to kin
(Osorio-Beristain and Drummond,
1993; Schjørring,
2001; but see Fischer,
1976).
Here, we show that the settling pattern of barnacle geese Branta leucopsis females returning to their natal colony is non-random with respect to the nest sites of their parents and sisters. By analyzing proximity to sisters in the absence of their parents and by comparing sisters born in different years with sisters from the same brood, we were able to determine whether kin clustering is a by-product of extreme natal philopatry and whether barnacle geese are capable of recognizing kin that they have not been into contact with before. We show that there is a genuine preference for settling close to sisters, but that this is unlikely to arise through phenotype matching. We also investigated whether settling close to kin is beneficial in terms of territory acquisition or breeding success and here we discuss the apparent lack of evidence for kin selection in colonially breeding waterfowl and seabirds.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Fieldwork was carried out in the oldest and largest colony of the Baltic barnacle goose Branta leucopsis population, situated on the three islands of Laus Holmar off the East Coast of Gotland, Sweden (57°17' N, 18°45' E). This colony is the subject of a long-term study that started in 1984. In 1984 this colony consisted of 325 breeding pairs and increased rapidly to 2340 pairs in 1999. The Baltic barnacle goose population was naturally established in the beginning of the 1970s, most probably by birds originating from the much larger Arctic-breeding Russian population (Larsson et al., 1988
), and
consisted of about 17,000 individuals in 1997
(Larsson and van der Jeugd,
1998). Because of strong density-dependent effects, reproductive
success per pair in the study colony is now very low
(Larsson and Forslund, 1994),
and females delay the start of reproduction until they are, on average, almost
4 years old (van der Jeugd,
1999). Natal philopatry is high in females, with on average 80% of
surviving females returning to breed in their natal colony. Male natal
philopatry is lower and varies between 30 and 55% (van der Jeugd,
1999,
2001). Barnacle geese are
precocial, and newly hatched chicks leave their nest site within the first 1
or 2 days of their life. Parents then take their young to brood-rearing areas
where the young grow to fledging size in 6-8 weeks. In our study colony, one
brood-rearing area is situated on the largest of the three breeding islands;
two other areas are farther away. Families remain intact during most of the
offspring's first winter. Nest sites of pairs in which at least one bird was marked were mapped on 1:2000 maps on the two largest of the three breeding islands. On the smaller island (13.2 ha) this was done in 1988, 1990, and 1994 (part of the island only), and on the larger island (39.7 ha) in 1987 (part), 1988 (part), 1994, 1995, 1996 and 1997 (part). We mapped the position of the nest site for 792 breeding pairs in at least one year (range 1-6 years) from hides at the edge of the breeding islands. Positions were then translated into x- and y-coordinates to the nearest 5 m. Repeatability of x- and y-coordinates for 84 pairs that were known to have bred at exactly the same site in 1995 and 1996 because nests were directly adjacent to landmarks was high (x-coordinate: ri = .996 F83,167 = 508.83, p < .0001; y-coordinate: ri = .989 F83,167 = 187.11, p < .0001). The median distance between two estimated positions of the same nest site was 20 m, with a maximum of 86 m. We therefore assumed that only pairs that had nest sites more than 86 m apart in 2 successive years had actually changed nest site from one year to the next, and found that pairs had changed nest sites between successive breeding attempts in only 17 out of 460 cases (3.7%) where a pair was recorded in 2 successive years. Thus, we assumed that the natal nest site of individuals generally had the same position as the nest site of their parents recorded in a later year.
To reduce effects of interyear and interobserver differences, we calculated
the distance between nest sites of related birds in the first year in which
the nest sites of both birds were recorded simultaneously. When this was not
possible, the distance was calculated using the mean position of the two nest
sites using all available years. To test for nonrandom settling with respect
to kin, randomization tests were performed by comparing the actual mean
distance between nest sites of related birds to the distribution of mean
distances obtained by randomly allocating relatives to each other within the
same sample for 5000 times. This procedure was repeated for all classes of
related individuals (Adams and Anthony,
1996). All randomization tests were two-tailed.
To distinguish between natal philopatry and preferences for breeding close to kin, we analyzed the distance between nest sites of siblings that had settled on a different island than where the nest site of their parents (i.e., the natal nest site) was located. We also compared the distance between nest sites of siblings born in the same year with the distance between nest sites of siblings that had the same parents but were born in different years.
Because only nests where at least one member of the pair was marked were
mapped, we do not know exactly how many territories were in between the nests
of two related birds. However, the total number of nests was known for each
island in each year, and average territory size could be calculated by
dividing the area of the island by the number of nests present for each year.
The average distance between two neighboring nests, in meters, was then
approximated by 2(A/
), where A stands for territory size
in square meters.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Females nested significantly closer to their parents than expected (Figure 1A; mean distance = 212 m, n = 53, randomization test: p < .0002), but nest sites of males conformed to a random pattern (Figure 1A; mean distance = 392 m, n = 28, randomization test: p = .2576). Sisters also nested closer to each other than expected at random, but only when born in the same year (Figure 1B, same year: mean distance = 188 m, n = 19, randomization test: p < .0002; different year: mean distance = 326 m, n = 17, randomization test: p < .3026). Sisters did not nest closer to brothers born in the same or in a different year, and brothers born in the same or different years did not nest closer to each other than expected at random (mean distances = 315, 362, 471, and 360 m, n = 18, 13, 2, and 4, respectively, randomization tests: all p > .3). Because the nonrandom settlement of sisters could be an effect of sisters settling close to their parents and thereby also close to each other, we examined the distance between nest sites of sisters that had settled on a different island while their parents remained breeding on the natal island. Again, we found that these sisters nested closer to each other than expected if they had settled at random when born in the same year (mean distance: 135 m, n = 10, randomization test: p < .0002), but there was no tendency among sisters born in different years (mean distance 347 m, n = 11, randomization test: p = .5436).
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On the smaller island, where the number of breeding pairs was stable from 1988 to 1994, the average distance between nests was 21 m for years in which nests were mapped. On the larger island, where the number of breeding pairs increased from 290 in 1987 to 1600 in 1997, the average distance between nests decreased from 42 to 18 m (average 26 m). From this it can be inferred that 10% of females settled next to their parents, while 12% of females settled next to a sister. The median number of territories that separated parents and daughters, or two sisters was 5. No cases of breeding pairs consisting of two closely related individuals were found.
Birds that were reared in the breeding colony (i.e., had been foraging with their parents in the vicinity of their natal nest site from hatching to fledging) did not settle closer to their parents (on the natal nest site) than birds reared at more distant sites (i.e., birds that had been near their natal nest site only during the first days of their lives; ANOVA: F1,79 = 0.02, p = .9).
The distance between parents and daughters was not related to the
daughters' age at first reproduction (linear regression:
F1,51 = 1.22, p = .3) or to the relative mean
number of young that fledged annually (linear regression:
F1,36 = 0.01, p = .9). Neither did sisters that
nest close to each other recruit earlier in life (linear regression:
F1,21 = 0.12, p = .7), and there was an almost
significant tendency for sisters that bred close to each other to produce
less, instead of more, young (linear regression: F1,18 =
4.19, p = .06). However, these analyses lacked statistical power, and
the probability of finding a medium effect (d = 0.3) varied between
27% and 61% (Cohen, 1988).
A possible mechanism explaining the clustering of sisters born in the same
year could be that such sisters settle as a "team." However, eight
pairs of sisters that settled within 200 m from each other did not settle in
the same year more often than eight pairs of sisters that settled more than
200 m away from each other did (
22 = 3.09
p = .21).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We have shown that female barnacle geese that returned to breed in their natal colony settled close to the nest site of their parents and sisters. Because breeding birds rarely changed nest sites between years, this natal philopatry could be caused by an attraction to the natal nest site itself or to the parents nesting there. However, females that settled on a different island than where their parents bred still settled close to their sisters. This clearly demonstrates that sisters nesting close to each other is not a by-product of either extreme natal philopatry or a preference to nest close to parents, but results from a genuine preference for nesting close to kin. It has been shown for a number of species that one sex settles closer to kin than the other (Lambin and Yoccoz, 1998
; Mappes et al.,
1995; Piertney et al.,
1999; Pusenius et al.,
1998; Schjørring,
2001; Spear et al.,
1998), but few attempts have been made to tease apart effects of
extreme natal philopatry and preferences for kin (but see
Schjørring, 2001).
However, even if kin clustering does not result from direct preferences for
breeding close to kin, limited dispersal of one sex can promote social
organization in populations, and a preference for the natal environment might
be used as an indirect method of settling close to kin in highly philopatric
species (Lacy and Sherman,
1983).
Sisters only nested close to each other if they were born in the same year.
In other words, females only nest close to sisters that they have been in
close contact with. Moreover, by preferring to nest close to familiar brood
mates, females may often not nest close to kin because 17% of brood mates
result from intraspecific nest parasitism or adoption
(Larsson et al., 1995).
Unfortunately, our sample sizes are too small to check whether unrelated
female brood mates nest as close to each other as real sisters. Little is
known about the mechanisms by which animals can recognize and discriminate
between kin and non-kin (Komdeur and
Hatchwell, 1999). The data we have presented here seem to imply
that barnacle geese do not use a mechanism such as phenotype matching by which
they can recognize unfamiliar kin (Komdeur
and Hatchwell, 1999; Lacy and
Sherman, 1983), but only discriminate familiar brood mates, which
they presumably know well because barnacle geese families remain intact for
much of the offsprings' first year of life. Our findings corroborate the
earlier finding that barnacle geese prefer to pair with familiar associates
from early life, but not with unfamiliar individuals from the same genetic
stock and with similar head patterns
(Choudhury and Black,
1994).
It may not be surprising that barnacle geese do not cluster with unfamiliar
kin. First, because brood mates are frequently not related to each other, only
self-referent phenotype matching (i.e., learning one's own phenotype and
comparing this with the phenotype of unfamiliar individuals) can lead to
reliable identification of unfamiliar kin. The likelihood of self-matching
mechanisms actually occurring is still controversial (but see
Mateo and Johnston, 2000).
Second, the reliability with which a character reflects underlying genes, and
thus its value in phenotype matching, decreases when the influence of
environmental factors on its expression is large
(Lacy and Sherman, 1983). It
has previously been shown for our study population that conditions experienced
during growth can have large effects on the adult phenotype, for example, on
different morphological traits (Larsson et
al., 1998). Phenotypic characters may therefore not be reliable
enough for phenotype matching to work across cohorts in barnacle geese.
Females could potentially learn the location of their natal nest site.
However, this is unlikely because chicks leave their nest site within the
first 1 or 2 days of their life, and females that were reared close to their
natal nest site did not settle closer to it compared to females that were
reared at a different site some kilometers away. Rather, we suggest that
females actively can seek out their parents and sisters and then settle close
to them. Sisters that settled close to each other probably did not settle as a
team, as they usually did not settle in the same year.
We were not able to show that settling close to the natal or parental nest
site or close to a sister's nest site were beneficial in terms of territory
acquisition or breeding success. However, because sample sizes were small and
because many other factors influence age at first reproduction and breeding
success (e.g., population density, birth year, age, and body size), these
analyses lacked statistical power. Furthermore, there are likely to be
conflicts between males and females over how to behave toward neighbors.
Although females might be related to other females nesting close by, males are
likely not to be related to their neighbors because they are less likely to
return and breed in the natal colony (van der Jeugd,
1999,
2001), and returning males
settle at random with respect to kin (this study). This also points to a
rather unique aspect of this study: in barnacle geese, pair formation takes
place before territory establishment, and there must therefore be some form of
communication from the female, who decides where a territory is to be
established, to the male, who actually establishes and defends this
territory.
At present, we do not know whether the observed settling patterns of
females (Figure 2) are biased
enough to lead to an ecologically significant matrilineal colony structure
with female relatives nesting close together. Variation in the distance
between related females was large, and assuming an
immigration—emigration balance, 20% of the females that settle each year
originate from a different colony (van der Jeugd,
1999,
2001). The application of
molecular markers such as microsatellites is the only way to investigate the
spatial pattern of relatedness among females in this colony of barnacle geese.
Application of such techniques has confirmed that natural populations can be
more or less subdivided into clusters of close relatives (e.g., Girman, 1997;
Piertney et al., 1999;
Pope, 1998;
Surridge et al., 1999). If a
matrilineal colony structure indeed exists, this might imply that behaviors
such as egg dumping and adoption, which occur frequently in our study colony
(Larsson et al., 1995), may
occur more often between related females than expected at random (see
Andersson and Åhlund,
2000; Bukacinski et al.,
2000).
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Most colonially nesting seabirds and waterfowl share ecological and
life-history characteristics that recent modeling
(Kokko and Lundberg, 2001) as
well as phylogenetic (Arnold and Owens,
1998) and interspecific studies (reviewed in
Hatchwell and Komdeur, 2000)
have found to be important for the evolution of kin-selected cooperation: They
are longlived, highly philopatric, and access to nest sites is limited. Yet,
helping behavior has been documented for only one species of seabird, the
brown skua Catharacta lonnbergi
(Millar et al., 1994), and,
curiously, helpers are usually not related to other members of their social
group in that species (Young,
1998). It has been proposed that seasonality in breeding should
select against the evolution of cooperation because, in migratory species,
groups may disband (Arnold and Owens, 1999;
Kokko and Lundberg, 2001).
However, in geese, offspring remain with their parents during most of their
first winter and may sometimes even associate with their parents during
subsequent winters (Ely, 1993;
Fox et al., 1995;
Scott, 1980; van der Jeugd,
unpublished data). It also seems likely that seabirds, although probably
dispersed outside the breeding season, could nevertheless find each other
again once they return to the natal colony.
For helping to pay off, it should have an effect on offspring production or
on survival of parents. Although helping at the nest obviously is not an
option in waterfowl because they do not feed their young, help with guarding
small young against predator attacks or the joint defense of high-quality
grazing grounds could potentially influence breeding success. Currently, there
are few studies of kin clustering and kin-based cooperation in colonially
breeding seabirds and waterfowl, but most of these do point into the direction
of clustering of kin occurring and possibly being beneficial
(Bukacinski et al., 2000;
Fischer, 1976;
Osorio-Beristain and Drummond,
1993; Schjørring,
2001; Spear et al.,
1998; Young,
1998). The evolution of coloniality has been intensively studied
during the past three decades, but no general conclusion can be given
concerning its evolutionary function
(Danchin et al., 1998;
Rolland et al., 1998).
Benefits arising through kin selection might be an additional important
factor, and future research should be directed to analyzing patterns of
relatedness and interactions between related individuals within colonially
breeding birds.
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ACKNOWLEDGEMENTS |
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The help of Pär Forslund during the earlier years of this study is greatly acknowledged. We also thank the field assistants who have helped us observe barnacle geese on the breeding grounds. Leo Bruinzeel and Martijn van de Pol helped with the randomization tests. Leo Bruinzeel, Hanna Kokko, Solveig Schjørring, and Ben Sheldon made valuable comments on the manuscript. Financial support was provided by the Swedish Research Council and the Swedish Environmental Protection Agency (grants to K.L.), and by the Olle och Signhild Engkvist Stiftelser, Stiftelsen för Zoologisk Forskning and the Royal Swedish Academy of Sciences. H.J. was supported by a grant from the Swedish Foundation for International Cooperation in Research and Higher Education (STINT) while in Oxford.
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