page provide an introduction, with references, to some of our current
research topics in barn swallows.
Enlargements of all the photos can be obtained by clicking on them.
Barn swallows are small passerine birds belonging to the family of
swallows and martins Hirundinidae. They weigh ca. 20 g, and most morphological
characters are similar in males and females, with the exception of
the outermost tail feathers which are longer in males than in females
(5% difference in North Africa increasing to almost 25% in Northern
Barn swallows are socially monogamous, with males arriving to the
breeding grounds before females. Arrival occurs in Southern Europe
in March-April and in Northern Europe later until June. After establishing
a small breeding territory, males attempt to attract a mate by flight
displays and showing off their long tail feathers. Once established,
the male and the female build a nest of mud pellets, where the female
will lay 3-7 eggs, usually 4-5 eggs. The female incubates the eggs
ca. 14 days (in North America males also incubate), and the nestlings
are fed ca. 21 days before fledging. They are fed by the adults yet
another week before becoming independent. The number of broods ranges
from one in Northern Europe to three in Southern Europe. Fledglings
roost in communal roosts in reed beds or similar sites, where more
than 100,000 birds can sleep together. Adults join roosts later in
autumn. Migration takes place in Northern Europe in September-October
and in Southern Europe in August-September. In Southern Spain and
Northern Africa breeding birds may return already in January-February
and they leave again already in July-August.
swallow nest-building in south-western Spain.
a barn swallow's famoulsy elongated tail near Chernobyl in Ukraine
(Anders Pape Møller and Tim Mousseau)
Males have longer outermost tail feathers than females, and males
enjoy an advantage in terms of mating success because of this effect.
Long-tailed males are more often mated (Møller 1994), mate
more quickly (Møller 1988, 1990, 1991, 1994), have more broods
(Møller 1988, 1990, 1994), have females that provide more parental
care (Møller 1991; de Lope and Møller 1993), and have
more extra-pair copulations than other males (Møller 1988).
Male barn swallows also have other characters involved in sexual selection,
including white tail spots on the tail feathers (Kose and Møller
1998; Kose et al. 1999), symmetric tail feathers (Møller 1992,
1994, 1995), a red facial plumage (Ninni et al. unpublished), and
a high song rate (Møller et al. 1998).
different traits are positively correlated, implying that they are generally
indicating the same quality properties. Several of the traits have also
been shown to be condition-dependent. Male tail length and tail asymmetry
also have significant resemblance among relatives (Møller 1991,
tend to work harder when mated to attractive males. Such differential
parental investment is a maternal effect that provide attractive males
with a selective advantage (de Lope and Møller 1993; Møller
Long tails are condition-dependent secondary sexual characters, with long-tailed
males surviving better (Møller 1991, 1994; Møller and Nielsen
1996). However, when tail length is manipulated, an experimental increase
in tail length causes a reduction in survival, while a shortening in tail
length causes an increase in survival (Møller and de Lope 1994).
Migration is much faster in spring than in autumn, with males and
to some extent females competing for early arrival and hence access
to preferred partners (Møller 1994). Males with long tails
arrive earlier than others, and condition-dependent arrival date
results in such males have a large advantage in terms of start of
breeding and hence in annual reproductive success. Arrival date
is heritable and there is a genetic correlation between arrival
date and male tail length (Møller 2001).
Barn swallows from Europe and western parts of Asia mainly winter
in Africa south of the Sahara. Birds from different parts of the breeding
range winter in different parts of Africa. Survival rate is affected
by rainfall in the African winter quarters (Møller 1989).
Weather conditions in the African winter quarters directly affect
the annual survival rate of adult barn swallows from the Danish population
(A. P. Møller and T. Szép unpublished data). Mortality
during the rapid spring migration can be considerable in Northern
Africa, mainly so in years when rainfall in the winter quarters have
been low (A. P. Møller and T. Szép unpublished data).
Thus, there is an added negative effect of poor weather conditions
in Southern Africa on mortality during migration.
in Africa have an important effect on barn swallow survival rate.
Clutch size, breeding date, egg size, number of clutches, and survival
are life history characters that together in a given combination may provide
an optimal solution to partitioning of reproductive effort under given
We have investigated clutch size decisions by manipulating clutch through
an increase by one egg or a decrease by one egg. These small manipulations
change the effort of attending parents, but also affects the quality of
the resulting offspring (Saino et al. 1997, 1999). Importantly, when parental
effort is increased, this reduces the probability of survival from one
year to the next (Saino et al. 1999).
Parasites play an important role in mediating the costs of reproduction
in barn swallows. Parasites may affect the optimal clutch size because
parents may be able to rear a different number of offspring when parasitised
than when free of parasites (Møller 1991), and also their quality
and quantity (de Lope and Møller 1993). In an experiment in which
both clutch size and mite load of nests were manipulated experimentally,
parasites increased the within-season costs of reproduction by reducing
the frequency and delaying the start of second clutches (Møller
Spanish barn swallow.
When barn swallows become old, they tend to have reduced survival
rates and deteriorate in quality. This is reflected by their tails
and wings starting to become shorter, their parasite loads increasing,
their arrival date becoming retarded, clutch size decreasing, and
parasite loads increasing (Møller and de Lope 1999). Parental
investment during the first year causes a reduction in reproductive
performance in subsequent years, and the quality of offspring in terms
of a component of immunity in one year is negatively related to the
quality of offspring the subsequent year (Saino et al. 2001).
Barn swallows are colonial passerines that often reuse their nest sites
from one year to the next. Hence, nests are often infested with large
number of ectoparasites such as mites, fleas, louseflies and feather lice.
Several populations also have high levels of helminth infections. The
number of parasites build up over the breeding season (de Lope and Møller
1993). This is associated with a change in priority of nestling development
from growth to immune function when comparing first and second broods
(Merino et al. 2000).
Presence of blood sucking mites causes barn swallows to build new nests
(Møller 1990). Mites reduces reproductive success and the quality
of offspring produced, and second broods are reduced in frequency and
delayed by mites (Møller 1990). Louseflies likewise reduce the
quality of offspring produced (Saino et al. 1989). Barn swallows have
relatively large reductions in reproductive success caused by parasites,
as compared to other hirundines (Møller et al. 2001).
suck blood from both adults and nestlings. Males with long tails have
fewer mites than the average male (Møller 1990, 1991), and many
mites reduce the length of the tail and increase the asymmetry of the
tail after the subsequent moult (Møller 1990, 1992). Mites are
less able to suck blood from the offspring of long-tailed birds, and their
reproductive rates are reduced (Møller 2000). The abundance of
mites has decreased dramatically during the last 15 years, as tail length
in the adult barn swallows has increased (Møller 2001).
A barn swallow
landing on its nest, showing the white spots on the tail feathers
which are the preferred habitat of feather lice.
lice and feather mites are common on nestling and adult barn swallows
(Møller 1991). Males with long tails have fewer feather lice
(Møller 1991), and so do males with large white spots on
their tails (Kose and Møller 1999; Kose et al. 1999). Feather
lice preferentially eat parts of the feather that are white, and
habitat choice experiments have shown that they prefer this part
of the feather (Kose and Møller 1999; Kose et al. 1999).
Feather lice seem to time their reproduction in response to testosterone
levels of their hosts, with experimentally increased testosterone
causing an increase in abundance (Saino and Møller 1995).
Nestling barn swallows attempt to avoid ectoparasites by fledging
early when a nest is heavily infested (Møller 1990). This
is achieved by changing growth priorities from skeletal traits to
feathers (Saino et al. 1999).
Barn swallows have relatively strong immune responses compared to solitarily
nesting hirundines (Møller et al. 2001). We have measured immunoglobulins,
T-cell mediated immunity and B-cell mediated immunity in adult and nestling
barn swallows. T-cell mediated immunity in nestlings is reduced by an
experimental increase in clutch size (Saino et al. 1997). When nestlings
are provided extra nutrients (from a small amount of beef), they increase
their T-cell response considerably (Saino et al. 1997). Parent birds trade
their own survivorship against the T-cell mediated immunity of their offspring
(Saino et al. 1999).
length of male barn swallows reflects B-cell mediated immunity, and females
may thus gain information on immunity of potential mates from their tail
length (Saino and Møller 1996). This measure of immunity provides
reliable information about male quality because males with strong responses
were better able to survive the annual migration to Africa than were those
with weak responses (Saino et al. 1997).
Immunoglobulin levels of adult barn swallows fluctuate in relation to
the time of the reproductive cycle. Females show a peak during the period
just prior to and during egg laying, while males do not show a similar
pattern (Saino et al. 2000). Interestingly, females show a more dramatic
increase when mated to a very attractive male, suggesting that females
increase immunoglobulin levels as a way of increasing investment in maternal
antibodies in their eggs (Saino et al. 2000).
Carotenoids have physiological functions related to immunity and free
radical scavenging. If carotenoids are in short supply through the diet,
we should expect that males with bright red facial coloration to be in
prime health state. This prediction was supported in a study of immunoglobulins
and leukocytes in Italian breeding barn swallows (Saino et al. 1999).
Male barn swallows produce an elaborate song that is used for attracting
females. Males with experimentally increased mite loads reduced their
song rate (Møller 1991). Subsequent studies revealed that features
of the song reflect testosterone levels of males, but also information
about their social environment (Galeotti et al. 199). Male song also provides
information about health status since males with particular songs have
low levels of circulating immunoglobulins and leukocytes (Saino et al.
COMPETITION AND EXTRA-PAIR PATERNITY
Barn swallow females are constrained in their mate choice because
only a single female may become mated with a very attractive male
in a monogamous mating system. Hence, we should expect such females
to copulate with already mated males. Males with long tails are more
successful in obtaining extra-pair copulations than other males (Møller
1991), and experimental manipulation of tail length of males causes
a parallel change in extra-pair mating success (Møller 1988).
Extra-pair copulations result in extra-pair paternity, and males with
experimentally elongated tails sire more offspring in their own nests
and in other nests than control males (Saino et al. 1997). Male song
rate reduces the risk of extra-pair paternity, but more so for short
tailed than for long tailed males (Møller et al. 1998). Males
with a high frequency of extra-pair paternity in their nests feed
their nestlings relatively less than when their brood has less extra-pair
paternity (Møller and Tegelström 1997).
about to copulate.
A brood of barn
swallows begging in south-western Spain, showing their brightly colored
gapes which appear to be a signal of health.
AND NESTLING PHENOTYPE
Barn swallow nestlings beg vigorously for food from their parents
by producing loud calls and displaying their bright orange gapes.
The gape display is a reliable signal of health status since a challenge
of the immune system with sheep red blood cells reduces the level
of coloration, while artificial provisioning with lutein (the carotenoid
causing the coloration) increases the level of coloration (Saino
et al. 2000). Parent barn swallows respond to experimental manipulation
of gape colour by changing their allocation of food (Saino et al.
2000). Gape coloration reflects the viability of offspring (Saino
et al. 2001). Nestling begging calls also reliably reflect health
status (Sacchi et al. 2001). Both current hunger status and long-term
condition of nestlings affect their begging rate and the response
of parents to the displays (Saino et al. 2000).
Studies of micro-satellites in the barn swallow have revealed one
of the most variable molecular markers discovered (Primmer et al.
1995, 1996). The very high mutation rates have allowed direct description
of the modes of mutation (Primmer et al. 1996, 1998), and studies
of changes in germline mutation rates caused by low levels of radiation
in Chernobyl (Ellegren et al. 1997).
We have made many analyses of quantitative genetic variation in
phenotypic traits, and we have found evidence of significant heritability
of characters such as tail and wing length, abundance of ectoparasites
and social environment (Møller 1991, 1994, 2001; N. Saino
et al. unpublished data).
Barn swallows are common breeding birds in the area surrounding the
radioactive contaminated sites near Chernobyl, Ukraine. Our studies
have shown that barn swallows around Chernobyl have markedly elevated
levels of asymmetry in tails and wings compared to museum samples
from the same area before the contamination in 1986, and that birds
from control areas (Møller 1992). Mutation rates in micro-satellite
molecular markers are increased by a factor 5-10 over the rates in
control areas (Ellegren et al. 1997). The red facial plumage of barn
swallows consists of carotenoids, and birds from Chernobyl have much
paler coloration that birds from other areas, in particular males
(Camplani et al. 1999). The frequency of partial albinism of the red
facial plumage of a genetic origin occurs at a rate of ca. 15% in
Chernobyl, but at less than 1% elsewhere (Ellegren et al. 1997; Møller
and Mousseau 2001). Birds from Chernobyl tend to be smaller than other
birds, but since the size of barn swallows has not changed during
the period 1991-2000, these must be selected against (Møller
and Mousseau 2001).
Swallows from near Chernobyl: the bird on the left is partially
Barn swallows have shown long-term changes in phenotype that can be related
to changes in climate. A recent study showed that the relative importance
of first and second clutches in a Danish population changed in response
to changes in the North Atlantic Oscillation (NAO; Møller 2001).
When the NAO index was high, implying rainy weather in Northern Europe,
barn swallows produced low quality offspring in first broods, but high
quality offspring in second broods. The reverse was the case when the
NAO index was low and weather was sunny and warm early during the summer
in Denmark (Møller 2001). Immigration to the study population increased
following a year when annual productivity was caused mainly by fledglings
from the first brood. This implies that increases in NAO increases the
size of the barn swallow population through effects on the relative productivity
of first broods.
Barn swallows have changed dramatically in phenotype in Denmark during
the last 18 years, and this change appears to be associated with a micro-evolutionary
change in phenotype, with males having increasingly long outermost tail
feathers (A. P. Møller and T. Szép unpublished data).
Catching barn swallows
breeding in a barn in Ukraine (Tim Mousseau and Alexander Peklo).
Barn swallows are closely associated with humans and dairy farming
in most parts of the range. Hence, changes in farming practice have
resulted in reductions in reproductive success and quality of offspring
produced (Møller 2001). The number of cattle and the number
of recent years with cattle are good predictors of population size
on Italian and Danish farms (Ambrosini et al. 2001).
Population size has been decreasing in areas in Denmark, Germany and
other countries. Based on demographic models and individual histories
of recruitment and survival the breeding population in Northern Denmark
has been predicted to go extinct with a high probability during the
next few decades (Engen et al. 2001).