The Barn Swallow 9781472596888

Citation preview

14639.qxd

24/1/06

3:53 pm

Page 8

List of figures Chapter 1 Figure 1.1

Breeding and main wintering ranges of the Barn Swallow

21

Drawing of a Barn Swallow making a left-hand turn to catch an insect The proportional use of vegetated field boundaries by foraging Barn Swallows in good and bad weather Insect abundance in various habitats and habitat use by radio-tagged Barn Swallows in Switzerland in good and bad weather

31

Chapter 2 Figure 2.2 Figure 2.2 Figure 2.3

43 44

Chapter 3 Figure 3.1 Figure 3.2 Figure 3.3

The number of pairs of Barn Swallows and of immigrants settling at a site in relation to the number of old nests at the site Sonagram of type A and type B song of a male Barn Swallow Repertoire of syllables in the songs of an Italian Barn Swallow population

59 61 62

Chapter 4 Figure 4.1 Figure 4.2

Time taken to get a mate for male Barn Swallows with experimentally shortened, elongated or unaltered tails Relation between tail length of male Barn Swallows and the parasite load and longevity of their offspring

71

Number of offspring of male Barn Swallows with experimentally shortened, elongated or unaltered tails Frequency of infanticide in relation to the number of unmated males and population size

88

74

Chapter 5 Figure 5.1 Figure 5.2

94

14639.qxd

24/1/06

3:53 pm

Page 9

Chapter 6 Figure 6.1 Figure 6.2

Numbers of Barn Swallows recorded on grazed or ungrazed pasture and arable fields on Breeding Bird Survey plots Frequency of new nests built for second clutches in relation to mite numbers in nests of first clutches

106 111

Chapter 7 Figure 7.1 Figure 7.2 Figure 7.3

Decline in clutch size over the season at Stirling, Scotland Clutch size in relation to the North Atlantic Oscillation index Duration of incubation in relation to clutch size

119

Growth of Barn Swallow chicks in good and bad weather Contribution of male Barn Swallows to chick feeding Amount of food provided per chick in relation to brood size

131 139 140

Fledgling production of Barn Swallows in relation to age Reproductive success of Barn Swallows in relation to prevalence of mites Probability of recruitment of Barn Swallow chicks in relation to date of fledging Probability of survival of male and female Barn Swallows in relation to the immunocompetence of their offspring

154 160

120 126

Chapter 8 Figure 8.1 Figure 8.2 Figure 8.3

Chapter 9 Figure 9.1 Figure 9.2 Figure 9.3 Figure 9.4

164 165

Chapter 10 Figure 10.1

Figure 10.2 Figure 10.3

Change in arrival date of Barn Swallows between years in relation to the change in environmental conditions (the normalised difference vegetation index) in the winter quarters Arrival dates of Barn Swallows in Britain since 1959 and the average February–April temperature Pre-migratory weights of Italian and Spanish Barn Swallows

179

180 190

14639.qxd

24/1/06

3:53 pm

Page 10

Chapter 11 Figure 11.1 Figure 11.2

The decline in the Barn Swallow population in the Kraghede area of Denmark since 1984 Population trend of the Barn Swallow in the UK for 1966–2003 from the Common Birds Census/Breeding Bird Survey

199 200

14639.qxd

24/1/06

3:53 pm

Page 11

List of tables Chapter 1 Table 1.1

The species and ranges of the Barn Swallow genus Hirundo

19

Chapter 2 Table 2.1 Table 2.2

Percentage composition of the diet of adult Barn Swallows in the breeding and non-breeding seasons Percentage composition of the diet of Barn Swallow chicks in good and bad weather

37 45

Chapter 3 Table 3.1

Population densities of Barn Swallows in various habitats and localities

54

Chapter 5 Table 5.1

Percentage of extra-pair chicks and percentage of broods with at least one extra-pair chick in various studies

87

Chapter 8 Table 8.1

Development of nestling and fledgling Barn Swallows

133

Chapter 9 Table 9.1 Table 9.2

Hatching and fledging success, the percentage of pairs with two broods and the number of fledglings per pair per year in various studies of Barn Swallows Survival rates of Barn Swallows

151 167

Chapter 10 Table 10.1

Dispersal distances between seasons of juvenile and adult Barn Swallows

194

14639.qxd

24/1/06

3:53 pm

Page 12

Chapter 11 Table 11.1

Local population declines in central Europe in the twentieth century

199

14639.qxd

24/1/06

3:53 pm

Page 13

Acknowledgements My fascination with hirundines started in the 1970s at Stirling, where I studied their foraging behaviour. David Bryant provided much inspiration and encouragement and I thank him, Chris Hails and Dave Waugh for invaluable advice and discussion from the start. I have had the pleasure of discussing hirundines with many people over the past 30 years and I thank them all for their help and insights. I also thank the farmers who allowed me to catch their Swallows and the Science Research Council for a studentship. I’m very grateful to the following for their help in answering queries or providing references or information: Roberto Ambrosini, Emilio Baldaccini, Dawn Balmer, Andy Bennett, Tim Benton, Rob Bijlsma, Charles Brown, Kate Buchanan, Javier Cuervo, Florentino de Lope, Karl Evans, Matthew Evans, Roy Frost, Paolo Galeotti, László Garamszegi, Edward Gavrilov, Diego Gil, Dimitri Giunchi, Martin Grüebler, Anders Hedenström, Ian Henderson, Hannu Kärkkäinen, Rodney Key, Lucinda King, Odmund Kleven, Patti Loesche, Piotr Matyjasiak, Pierfrancesco Micheloni, Anders Møller, Peter Newbery, Robert Nudds, Andrea Pilastro, Rob Robinson, Vadim Ryabitsev, Becca Safran, Nicola Saino, Luc Schifferli, Fred Sheldon, Tim Sparks, Tibor Szép, Maimie Thompson, Bennie van den Brink, Sally Ward. Simon and Pat Cox, Karl Evans, Paolo Galeotti, G. Higginbotham, Hannu Kärkkäinen, Tomi Muukkonen, Jari Peltomaki. Rob Robinson, Luc Schifferli, Fredrick Sears, Tim Sparks, Philip Stoddart, Bennie van den Brink, Markus Varesvuo and Sally Ward kindly provided photographs or figures. I am also grateful to the following for permission to reproduce copyright material: Blackwell Publishing (Figs 7.2, 7.3, 8.3, 9.1, 9.2, 9.4, 10.1, 10.3, 11.2); British Trust for Ornithology (Figs 2.2, 6.1, 11.1); Ecological Society of America (Fig. 6.2); Elsevier (Figs 3.2, 3.3); National Academy of Sciences, USA (Fig. 4.2b); Nature Publishing Group (Fig. 4.1); Oxford University Press (Figs 5.2, 8.2); The Royal Society (Fig. 2.1); The Society for the Study of Evolution (Figs 4.2a, 5.1); Springer (Fig. 9.3); University of Chicago Press (Fig. 3.1); Su Engstrand (Fig. 7.3); Karl Evans (Fig. 2.2); Paolo Galeolti (Figs 3.1, 3.2); Anders Møller (Figs 4.1, 4.2, 5.2, 6.2, 7.2, 8.2, 9.1, 9.2, 9.3, 11.2); Åke Norberg (Fig. 2.1); Rob Robinson (Figs 6.1, 11.1); Diego Rubolini (Fig. 10.3); Becca Safan (Fig. 3.1); Nicola Saino (Figs 5.1, 8.3, 9.4, 10.1); Luc Schifferli (Fig. 2.3). Several people generously commented on one or more chapters, for which help I thank Roberto Ambrosini, Kate Buchanan, Javier Cuervo, Florentino de Lope, Su Engstrand, Karl Evans, Paolo Galeotti, László Garamszegi, Dmitri Giunchi, Hannu Kärkkäinen, Odmund Kleven, Patti Loesche, Anders Møller, Åke Norberg, Andrea Pilastro, Diego Rubolini, Becca Safran, Nicola Saino, Luc Schifferli,

14639.qxd

24/1/06

14

3:53 pm

Page 14

The Barn Swallow

Tim Sparks, Karen Spencer, Maimie Thompson, Bennie van den Brink and Sally Ward. Jevgeni Shergalin and Mike Wilson kindly translated papers and helped with the Russian language literature. Carole Showell at the BTO Library and Linda Birch at the EGI Library helped with finding references. I am also grateful to Andy Richford at Academic Press for his encouragement and patience at the beginning, to Marianne Taylor, Nigel Redman and Jim Martin at A&C Black, who ably saw the book through its final stages, and to Ernest Garcia for his copy editing. Many thanks, too, to Ian Rendall for enhancing the text and cover of this book with his superb illustrations.

14639.qxd

24/1/06

3:53 pm

Page 15

CHAPTER 1

The swallows The hirundines are a most inoffensive, harmless, entertaining, social, and useful tribe of birds. Gilbert White, 1789

Barn Swallows are familiar birds in many parts of the world. Their willingness to nest and forage close to people has made them a part of the fabric of farmyard and village life. They are welcomed in spring, are a symbol of good luck and have a place in numerous legends and superstitions, as well as in poetry. They are popular among bird-ringers and scientists, too, and are among the most well-studied bird species in the world. The Barn Swallow is one of 83 species belonging to the Hirundinidae, the family of birds comprising the swallows and martins (collectively known as hirundines) (Turner 2004). These small- to medium-sized passerines, ranging from the 10 g White-thighed Swallow to the 60 g New World martins, are all specialist aerialfeeders, pursuing and catching insects in flight. Consequently, they look rather

14639.qxd

24/1/06

16

3:53 pm

Page 16

The Barn Swallow

similar with features such as a streamlined body, long wings and a forked tail that aid aerial hunting. Many have contrasting dark upperparts, often metallic blue or green, and paler white, buff or rufous underparts. They are also characterised by markings such as the red forehead and throat, the dark breast-band, and the white tail spots of the European Barn Swallow and the white rump of the Northern House Martin. Yet, despite these similarities, a fascinating diversity exists in their distribution, ecology and behaviour, between and sometimes within species. Hirundines occur almost everywhere except the Arctic and Antarctic, but are most diverse in sub-Saharan Africa where some 30 species breed. The extent of the species’ distributions varies widely, though. The White-tailed Swallow, for example, occurs in a range of less than 15,000 km2 around Mega and Yavello, in southern Ethiopia; in contrast, the Barn Swallow breeds in North America, Europe, North Africa, and northern and central Asia. Hirundines are also found in many types of habitat, as long as there is a place to nest and open areas for feeding. Many breed in grasslands, along rivers and by wetlands. Those that associate with people now inhabit farmland, villages and towns. Although absent from dense forest, some, such as the Square-tailed Saw-wing, breed in forest clearings. Others, such as the White-banded and Black-collared Swallows, breed along forested rivers. An intriguing aspect of the biology of hirundines is the way that many species build nests of mud. Others nest in pre-existing holes or make their own by burrowing. Although natural nest sites are still widely used by some species, others now use human artefacts, from nestboxes to bridges to our own homes. Indeed some, such as the Purple Martin and the Barn Swallow, now almost always nest in such sites. Another well-studied behaviour of hirundines is their sociality. Many species will nest close together and some, such as the Cliff Swallow, nest in large colonies. Only a few species, such as the Mangrove Swallow, are solitary nesters, defending a large territory. Although many hirundines are still poorly studied, we know a great deal about a few species, including the Tree Swallow, Purple Martin, Collared Sand Martin and Cliff Swallow. The Barn Swallow itself has had more scientific papers written about it than have other hirundines, and probably most other birds. Indeed there are too many studies to mention; consequently I refer to reviews, such as Cramp (1988) and Brown & Brown (1999a), as much as possible. There are many studies of the biology of local populations. There are also long-term projects considering wider issues such as why females choose certain males as mates and why males have long outer tail feathers. To give a flavour of the research on Barn Swallows, it is worth mentioning a few long-term studies. Since the 1970s, several aspects of the Barn Swallow’s biology, such as the energetics of breeding, have been studied at Stirling in central Scotland, and this is where I did my own study of the foraging behaviour of Barn Swallows (Turner 1980). In Denmark, Anders Møller has been studying Barn Swallows around Kraghede since 1971, initially looking mainly at mate choice and sexual selection and more recently factors affecting productivity and survival. There are also long-term studies in Spain and Italy on a variety of subjects such as songs, chick

14639.qxd

24/1/06

3:53 pm

Page 17

The swallows

17

begging and immune function. Møller and other scientists are now collaborating on comparative studies of Barn Swallows in Finland, Estonia, Hungary and Algeria as well as Denmark, Italy and Spain. Barn Swallows affected by radiation from the nuclear accident at Chernobyl are also under study. In North America there have been several studies, particularly in New York State and Nebraska, investigating, for example, the costs and benefits of living in a group. There has been little research on mate choice and sexual selection in North American Barn Swallows, compared with that on European ones, but recent and ongoing studies are making up for this lack of knowledge. Barn Swallows are also the focus of various small and large-scale ringing projects. The main study is the EURING Swallow Project, which started in 1998, with the aim of studying the species’ population dynamics and dispersal patterns.

EVOLUTION AND TAXONOMY Hirundines have a body design adapted for flight, and they form a distinctive family. As well as the streamlining of the body with a short neck and the long, pointed wings, hirundines have short legs with small, weak feet, and reduced leg muscles compared with other songbirds. The bill is short with a wide gape. The wings have ten primaries, with the outermost reduced. The tail has 12 rectrices and in many species it is forked, sometimes with elongated and narrowed outermost tail feathers. The tarsi are short and ridged at the back, and there is sometimes feathering on the toes and tarsi. A unique feature of typical hirundines lies in the structure of the syrinx, the resonating chamber at the bottom of the windpipe, which has more or less complete bronchial rings, instead of the half rings with a membrane at the front found in other songbirds. Two species, the African and White-eyed River Martins, though, stand out as being rather stocky with large bill, legs and feet; internally they have a large syrinx with half bronchial rings. Taxonomists thus put them in a separate subfamily. Because of the similarities in structure and behaviour of the different species, and their distinctiveness from other songbirds, taxonomists have found it difficult to determine the relationships of hirundines among themselves and with other birds. Features such as nest type and plumage patterns have been useful in determining genera, but there have still been areas of uncertainty. However, studies using molecular techniques have made considerable progress in understanding the phylogeny of hirundines (Sheldon & Winkler 1993; Winkler & Sheldon 1993; Sheldon & Gill 1996; Sheldon et al. 1999, 2005). The closest relatives of hirundines include the sylviid warblers, babblers, whiteeyes, tits and chickadees, and bushtits, from which they diverged some 50 million years ago. Hirundines probably originated in Africa and southern Asia as far as Australia and then expanded into Europe and the New World. Some closely related species provide evidence of this in their relict populations: the Grey-rumped Swallow

14639.qxd

24/1/06

18

3:53 pm

Page 18

The Barn Swallow

and the White-backed Swallow occur in Africa and Australia, respectively, and the river martins occur in Africa and south-east Asia, which suggests that their ancestors once had a more extensive distribution in Africa and Asia. The Grey-rumped and White-backed Swallows, along with the African saw-wings, are considered to be relict ‘primitive’ species. When hirundines extended their range beyond Africa and Asia is not known. The small fragile bones of hirundines rarely provide fossils, but a species (known as Hirundo aprica) resembling the Barn Swallow was present 3.3–3.5 million years ago in North America. The original hirundines probably excavated their own nest sites, as the modern sand martins do, burrowing into a riverbank or other soft substrate. They spread to the New World where they evolved into many genera that build nests in existing holes. These burrowing and hole-using hirundines are known as the ‘core martins’ and include a number of related groups: the Banded, Mascarene and Brazza’s Martins; the sand martins and tree swallows; the rough-wings and New World martins; and various endemic Neotropical genera. The remaining hirundines probably originated from nest-excavating species in Africa, and comprise the 38 species that build mud nests, including the Barn Swallow. The majority of these species have sometimes been included in a single genus, Hirundo, and sometimes split into several genera. The latest studies support the classification of mud-nest-building hirundines into five genera, grouped into two clades. One clade comprises the barn swallows belonging to the genus Hirundo and the crag martins in the genus Ptyonoprogne, which build open-cup nests; the other comprises the house martins (Delichon), the cliff swallows (Petrochelidon) and the red-rumped swallows (Cecropis), which build enclosed nests. The barn swallow group (the genus Hirundo) can be divided into three clades (Table 1.1). The Barn Swallow itself is one of seven similar species, which have glossy blue upperparts, white tail patches and, apart from the White-throated Blue Swallow, paler underparts, and rufous on the head and often on the throat as well. The Barn, Red-chested and Ethiopian Swallows are particularly closely related and the Red-chested Swallow has been considered conspecific with the Barn Swallow. The Pacific and Welcome Swallows have also been considered conspecific. The mud-nest-building hirundines have an advantage over hole-users and nestexcavators in that they can effectively build their own ‘hole’ and attach it to any vertical surface, in the absence of natural holes or soft substrates for burrowing. They have thus been able to breed in a variety of open habitats, as long as the climate is not too dry, when wet mud may be unavailable, or too wet, when the nest structure may be compromised. These species have spread from Africa and Asia into Australia, Europe and North America relatively recently and are continuing the invasion, with Barn Swallows now breeding, and Cliff Swallows attempting to breed, in South America.

14639.qxd

24/1/06

3:53 pm

Page 19

The swallows Table 1.1.

19

The species and ranges of the Barn Swallow genus Hirundo and their ranges.

Common name

Scientific name

Geographical range

Barn Swallow Red-chested Swallow Ethiopian Swallow

Hirundo rustica Hirundo lucida Hirundo aethiopica

Angolan Swallow

Hirundo angolensis

White-throated Swallow White-throated Blue Swallow Wire-tailed Swallow

Hirundo albigularis Hirundo nigrita Hirundo smithii

North America, Eurasia West & Central Africa, Ethiopia Central Africa, mainly north of the equator Equatorial Africa, mainly south of the equator Southern Africa West & Central Africa Africa, southern Asia

Barn Swallow clade

Pacific Swallow clade Pacific Swallow

Hirundo tahitica

Welcome Swallow

Hirundo neoxena

Southern India, south-eastern Asia, Pacific islands Australasia

Hirundo leucosoma Hirundo dimidiata Hirundo megaensis

West Africa Southern Africa Ethiopia

Hirundo atrocaerulea Hirundo nigrorufa

Southern and eastern Africa Angola east to Zambia

Pearl-breasted Swallow clade Pied-winged Swallow Pearl-breasted Swallow White-tailed Swallow Other species Blue Swallow Black-and-rufous Swallow

DISTRIBUTION AND VARIATION The Barn Swallow breeds in a broad band across Eurasia and North America, as far north as about 68° in Scandinavia and mostly to 63–66°N elsewhere (Figure 1.1). It occurs in a variety of habitats and climatic zones, being absent only from most of the Arctic tundra and from extensive areas of forest and deserts. Vagrants have reached many northerly points and oceanic islands such as northern Alaska, St Lawrence Island, the Pribilof and Aleutian Islands, Greenland, Jan Mayen, Bear Island, Spitsbergen, the Yamal Peninsula, Koryak Upland (north of Kamchatka), the Seychelles, the Hawaiian, Midway, Crozet and Falkland Islands, South Georgia and Tristan da Cunha (Kistchinskiy 1980; Danilov et al. 1984; Cramp 1988; Brown & Brown 1999a).

14639.qxd

24/1/06

20

3:53 pm

Page 20

The Barn Swallow

In the Old World, size and coloration of the underparts vary continuously, size declining from the northwest to the south and east (Cramp 1988). Eight subspecies are recognized (Figure 1.1). The nominate H. r. rustica Linnaeus, 1758 breeds in Europe and North Africa east to the Yenisey River, western China and the central Himalaya and winters mainly in sub-Saharan Africa. Breeding in the winter quarters is conceivable, as birds have been found in breeding condition in September in South Africa (A.P. Møller, pers. comm.). This is a large subspecies (wing length 125 mm in Scandinavia to 121 mm in Pakistan and northern India) with pale underparts, from buff-white to buff-rufous, and a full breast-band. Two subspecies have localised distributions in Africa and the Middle East: H. r. savignii Stephens, 1817 (wing length 119 mm) in Egypt and H. r. transitiva (Hartert, 1910) (male/female wing length 126/121 mm) in Israel, Lebanon, Jordan and Syria. Both have full breast-bands like rustica, but savignii has dark rufous-chestnut underparts and transitiva is a paler rufous-buff. The Asian subspecies, in contrast, have a narrow breast-band and also differ in the shade of the underparts. There is not a sharp distinction between the subspecies, however, and the form of the breastband varies clinally. Their breeding ranges require clarification. In eastern Asia, H. r. gutturalis Scopoli, 1786 is small (male/female wing length 116/115 mm) with pale creamy or white underparts. It occurs from the eastern Himalaya and southern, central and eastern China east to Taiwan, Japan and the Kuril Islands, and may breed irregularly in Kamchatka. It winters in southern and south-eastern Asia south to northern Australia. Birds in Sikkim, originally described as a separate subspecies ambigua, are sometimes included in rustica as they have an unbroken breast-band, but their size suggests they are probably nearer gutturalis (Dickinson & Dekker 2001). The darkest Asian subspecies, H. r. tytleri Jerdon, 1864 with uniform rufous-chestnut underparts (wing length 122 mm in Mongolia to 117 mm in southern Siberia), breeds in southern-central Siberia east to Yakutsk and south to northern Inner Mongolia, and winters from eastern India to south-east Asia. H. r. saturata Ridgway, 1883 (male/female wing length 116/115 mm) with rustyochre underparts breeds in Kamchatka south to the mid-Amur basin and east to the Sea of Okhotsk. It is not clear, however, whether breeding in Kamchatka is regular. H. r. mandschurica Meise, 1934 (male/female wing length 114/112 mm) with lightochre underparts breeds in north-eastern China. The subspecies saturata is often included in gutturalis or tytleri and mandschurica in saturata, although a recent comparison suggests the latter are separate (Dickinson & Dekker 2001; Dickinson et al. 2002). The Kamchatka population was also once designated a separate subspecies, kamtschatica Dybowski, 1883, but is now included in gutturalis/saturata. In westcentral Asia, rustica intergrades with tytleri, and tytleri also intergrades with eastern populations. In the lower Amur basin, it is likely that gutturalis is a recent immigrant, arriving with Russian settlers in the seventeenth century, and has hybridised with the Barn Swallows already there (Smirensky & Mishchenko 1981). The North American subspecies, H. r. erythrogaster Boddaert, 1783 (wing length 120 mm), breeds in North America from south Alaska, south Yukon, central-west Mackenzie, north Saskatchewan, north Manitoba, north Ontario, south-central

3:53 pm

Breeding and main wintering ranges of the Barn Swallow.

24/1/06

Figure 1.1.

14639.qxd Page 21

The swallows 21

14639.qxd

24/1/06

22

3:53 pm

Page 22

The Barn Swallow

Quebec and south Newfoundland south to north-west Baja California, Mexico south to Nayarit, Colima, Michoacán and Puebla, the Gulf Coast and north Florida. It is local or absent from only a few areas such as southern Florida, much of Arizona, south Nevada, south California, the higher parts of the Sierra Nevada in California, most of Baja California and coastal parts of Mexico (Brown & Brown 1999a). It winters in Central and South America and has also bred in Buenos Aires Province in Argentina since at least 1980 (Martinez 1983; Paynter 1995; Petracci & Delhey 2004). This subspecies has rufous-buff underparts and the breast-band is narrow and restricted to the sides of the breast. It is perhaps most similar to the east Asian subspecies, and indeed saturata, mandschurica and kamtschatica were once included in erythrogaster. The colour of the underparts is strongly variable both between and within populations, however (Cramp 1988). Darker birds can occur in a predominantly pale population and vice versa; for example, in Ukraine about 20% of birds have rufouschestnut underparts, in Italy more than 10%, in Denmark nearly 4% and in Spain fewer than 2% (Møller 1994a, pers. comm.). In North America, individuals occasionally have whitish underparts; pale-bellied Barn Swallows breeding on islands along the Gulf Coast have been considered a separate subspecies ‘insularis’ (Brown & Brown 1999a). Populations can be particularly variable where subspecies meet, such as rustica with transitiva, tytleri and gutturalis. The taxonomic relationships between members of the barn swallow group and between the various subspecies of the Barn Swallow are not clearly known. An analysis of mitochondrial DNA of Barn Swallows from North America and Magadan on the Sea of Okhotsk even suggested that erythrogaster, which differs in several respects from the Old World subspecies, could be viewed as a full species (Zink et al. 1995). A more recent DNA analysis found that the genetic divergence between the subspecies erythrogaster and rustica is almost as great as that between Barn Swallows, Red-chested Swallows and Ethiopian Swallows and these subspecies may be in the process of becoming full species (Sheldon et al. 2005). In contrast, a study of 15 European populations from Spain to Finland and Ukraine found no significant population divergence (A.P. Møller, pers. comm.). Although the mud-nest-building hirundines are split into five genera, their relatedness is shown by the occurrence of hybrids between them. Many possible cases of hybridisation between Barn Swallows and Cave Swallows, Cliff Swallows and, especially, Northern House Martins have been reported (and possible hybrids with Welcome and Red-rumped Swallows and Collared Sand Martin; Flumm 1975; Conole & Baverstock 1994; Heneberg 1997). Recent reviews noted over 270 Barn Swallow × Northern House Martin hybrids (Nicolau-Guillamet 1998; Kabus 2002) and many are being caught in the EURING Swallow Project. For example, extensive ringing in Finland between 1996 and 2002 turned up 156 hybrids (Saurola 2003) and several have been caught in Britain. Hybrids are regularly caught at roosts in Europe at low frequencies, ranging from about 0.13% in Finland to about 0.007% in Italy and Slovenia. Five breeding attempts by a presumed hybrid, and two broods with a possible hybrid parent, are known, but in no case was it certain that the hybrid

14639.qxd

24/1/06

3:53 pm

Page 23

The swallows

23

was a biological parent (Vansteenwegen 1981; Kabus 2002). Møller (1994a) suggested Barn Swallow × Northern House Martin hybrids are the result of Northern House Martin males forcing copulations on Barn Swallow females; hybrids between Barn Swallows and other species may also involve extra-pair copulations (Chapter 5) rather than different species pairing with each other (Brown & Brown 1999a). This idea is supported by the occurrence of hybrid chicks in nests with normallooking ‘siblings’ and, in one case, a complete brood of hybrids being reared by Barn Swallows (Martin 1980; Nicolau-Guillamet 1998; Kabus 2002; Saurola 2003; A.P. Møller, pers. comm.). Barn Swallows may have only recently come into extensive contact with Cave and Cliff Swallows, as the latter have expanded their range of nest sites to include culverts and bridges, where Barn Swallows also nest (Martin 1980). Hybridisation may be more likely in these circumstances. Hybrids vary in plumage, but typically have features reminiscent of both parents (Martin 1980; Nicolau-Guillamet 1998). They may, for example, have a pale forehead and throat, a breast-band and one or more white spots on the tail indicative of the Barn Swallow parent, but they also have features of the other species such as a pale or white rump and feathering on the tarsus in the case of Northern House Martins or a chestnut collar and buff or orange rump in the case of Cave or Cliff Swallows. Albino and pale (leucistic) Barn Swallows are occasionally seen, but dark (melanic) forms are rare; these individuals seem to be poorly tolerated by other Barn Swallows and to have poor prospects of survival (e.g. von Vietinghoff-Riesch 1955; Hoernecke 1990; Withgow & McMahon 1993; Whitford 1995; Ellegren et al. 1997; Bansemer 2001). An increase in partial albinism, that is, the presence of white feathers in plumage of normal coloration, has been noted in the Chernobyl region since the nuclear accident in 1986, associated with an increase in the germline mutation rate (Ellegren et al. 1997; Møller & Mousseau 2001): about 13–17% of birds between 1991 and 2000 had white feathers compared with none before 1986 and fewer than 2% in uncontaminated populations in Italy and elsewhere in the Ukraine.

SEX/AGE DIFFERENCES Males and females are similar in size, but differ in several respects (Cramp 1988; Thompson 1992; Møller 1994a; Møller et al. 1995c). Males have strikingly longer tails, with the outer tail feathers extending beyond the maximum tail span, whereas in females they do not; tail length is also more variable in males. Males and females differ to a lesser degree in other characters. Males have slightly longer wings, wider bills and longer keels. Females are larger than males in a few characters: they have slightly longer tarsi, central tail feathers and bills, larger throat patches and they also weigh more. Males have a slightly more intense blue plumage with greater ultraviolet reflectance (Perrier et al. 2002) and a much darker red coloration. In North

14639.qxd

24/1/06

24

3:53 pm

Page 24

The Barn Swallow

America, the rufous underparts from the throat to the vent are browner, more saturated and darker in males (Safran & McGraw 2004). The white spots in the tail are also larger in males; some females lack any spot in the second innermost tail feather (Kose & Møller 1999). The spots are larger in longer tails of both sexes and increase in size with age (Kose & Møller 1999). The fork length and the white patch on the outermost tail feather are often used to distinguish between males and females (Cramp 1988; Brombach 2004). The fork length, i.e. the difference between the tips of the inner and outer tail feathers, in European males is 47–80 mm, with only 4% less than 51 mm, whereas in females it is 27–57 mm, with 90% between 32 and 50 mm. The white patch on the outer tail feather is 20–35 mm long in males, with only 7% below 24 mm, and 11–26 mm in females, with only 10% over 23 mm. Thompson (1992) found that 94% of Scottish birds could be correctly sexed by their outer and inner tail lengths. Similarly, in North America, males have a fork of 35–53 mm and females have one of 26–38 mm (Pyle 1997). In addition, in five populations in Europe and Russia, the base of the outer tail feather was significantly wider in males (by 4% on average), whereas the tip of the feather was significantly narrower (by 10%). The base of the tail feather was more asymmetric around the vane in males, whereas the tip was less asymmetric (Møller et al. 1995c). Males also have a large cloacal protuberance, lack a brood patch during the breeding season, and have a characteristically darker red throat (A.P. Møller, pers. comm.). Both size and degree of sexual dimorphism vary geographically. The most studied subspecies in this respect is rustica: for both males and females, the wings and the central and outermost tail feathers are longer at higher latitudes (Møller 1995). Møller suggested that longer wings are an adaptation to having to fly further on migration. On average, the males’ outer tail feathers range in length from 90 mm to nearly 115 mm from south to north whereas those of females increase from 79 to 95 mm. The fork depth of males, but not of females, also increases from south to north, so that, for example, males in Spain have a tail only about 5% longer than females, in Italy 17% longer and in Finland more than 20% longer (Møller 1995; Møller et al. 1995c; Barbosa & Møller 1999a). In North America, there is a similar increase in outer tail length from lower to higher latitudes (averaging 79 mm for males and 73 mm for females in Mexico to 88 mm for males and 78 mm for females in Canada and Alaska; Brown & Brown 1999a). Sexual size dimorphism is generally similar for the different subspecies, although savignii shows little difference in tail length (7%, similar to Spanish rustica; Møller 1994a). The latitudinal differences between males and females also exist for the central tail feathers but not for wing length or tarsus length (Møller 1995). The central feathers are longer in tails with long outer feathers, but are relatively longer in females, and the difference between the sexes is smaller at high latitudes, in contrast to the difference in length of the outer tail feathers (Møller et al. 1995c). At higher latitudes, both males and females have more asymmetrical tails, that is, the two outermost feathers differ more in length and, in males only, tail length is more variable (Møller 1995). The latitudinal differences in tail morphology and in sexual

14639.qxd

24/1/06

The swallows

3:53 pm

Page 25

25

dimorphism within and between subspecies may be related to differences in climate, which in turn affect the Barn Swallows’ insect prey and foraging costs (Møller 1994a, 1995; Barbosa & Møller 1999b; Chapter 2). Before the first moult, young Barn Swallows have an orange forehead and throat rather than the rufous-chestnut of the adult. They have only faintly glossy, dark brownish-blue upperparts and wing coverts, the latter with pale edges, the breastband is mottled with buff, and the wings and tail are shorter than in adults. The outer tail feathers are less than 72 mm versus over 75 mm in European adults, and the fork length is less than 31 mm versus over 32 mm in adults (in North America the tail is less than 68 mm with a fork of 14–21 mm). In addition, the outer tail feather is broader (3.7–4.9 mm at the same level as the tip of the fifth tail feather versus 2.2–3.6 mm in adults) with a rounder white spot. The white tail spots are smaller than in adults (Kose & Møller 1999). Juveniles may resemble some adults in worn, and thus dull, plumage, but the paler forehead and throat and the short, broad outermost tail feathers with a rounded spot are distinctive. After the first moult, the plumage is indistinguishable from that of older birds, although first-years may sometimes retain a few worn juvenile feathers, usually pale feathers on the face, the outer tail feathers and the outer primaries, into their first summer. Juvenile females and males have very similar plumage until their first moult, although males tend to have blacker breast-bands and longer tail forks. As well as varying between males and females, wing and tail lengths change between years. In contrast, skeletal measurements, such as keel lengths, tend not to change with age (Thompson 1992). Size measurements are generally correlated, so that males with long tails tend to be large structurally, with long wings. The greatest increase in size occurs over the first two years. For example, in Scotland (Thompson 1992) wing length was 126.4 mm in one-year-old males, 126.7 mm in two-year-old males and 128.4 mm in males three or more years old, while for outer tail length the respective measurements were 101.5, 110.4 and 113.3 mm. Two-year-old females had longer tails (96.8 mm) than first-years (90.6 mm). The change in tail length between years for individuals ranged from −2 mm to +13 mm for males (mean 4.4 mm) and −1 mm to +10 mm for females (mean 2.5 mm), with 84% of males growing a longer tail between years. Similarly, Møller & de Lope (1999), studying Danish and Spanish Barn Swallows, found that tail length increased from age one to two years, by on average about 2 mm, and, to a lesser extent, from two to three years. Wing length also increased from age one to two years and decreased for old birds. The asymmetry in the length of the two outermost tail feathers decreased from year one to two, and both wing and tail asymmetry increased for old birds. Tail and wing length, however, are not reliable indicators of age, as individuals within an age class are variable in this respect. For example, Thompson (1992) found she could categorise only a third of males as first-years or older by their tail length. Those that she could age were at the extremes; those with tails of 90 mm or less were first-years, and those with tails of 114 mm or more were at least two years old.

14639.qxd

24/1/06

26

3:53 pm

Page 26

The Barn Swallow

The average size of birds in a population can also change, for instance when mortality hits a particular size class hardest. Brown & Brown (1999b) found that those Barn Swallows that survived a six-day period of cold wet weather in May 1996 were larger than those that died. Males that survived had significantly longer bills, whereas female survivors had long tails. Survivors also had more-symmetrical outer tail feathers. These differences in morphology might indicate that the survivors were of better quality and in better condition or that they could forage more efficiently (Brown & Brown 1999b). Thompson (1992) found differences in size between years: head-to-bill lengths of both sexes and outer tail length of males increased between the three years of her study. First-year size also varied between years, and females hatched in 1987 had significantly longer wings as first-years than those hatched in 1988. In a longerterm study, the average length of tails of males has changed in Denmark, although not in Italy or Spain, over the last 20 years, increasing from 103.5 mm in 1984 to 112.9 mm in 2004, whereas that of females changed only from 88.5 mm to 92.4 mm (A.P. Møller, pers. comm.). The change in tail length is related to feeding conditions on spring migration in North Africa (Algeria), and may be caused by fewer poorquality birds with short tails surviving adverse conditions, especially after making the journey across the Sahara (Møller & Szép 2005b). Feather growth depends on environmental conditions during the moult. Møller (1991d, 1994a) found that Danish males grow longer tails in a good winter with plenty of rain. Italian males also grow longer wings and tails, and females longer tails, when they have good feeding conditions on their wintering grounds (Saino et al. 2004c).

14639.qxd

24/1/06

3:53 pm

Page 27

CHAPTER 2

Flight and feeding behaviour Horsemen on wide downs are often closely attended by a little party of swallows for miles together, which plays before and behind them, sweeping around, and collecting all the skulking insects that are roused by the trampling of the horses’ feet. Gilbert White, 1789

Barn Swallows are specialist insect hunters, targeting large flies in particular when they have hungry chicks to feed, but also taking a range of small prey. They hunt almost exclusively in the air, and to that end are well adapted for low-cost, manoeuvrable flight, entailing frequent changes of direction.

14639.qxd

24/1/06

3:53 pm

Page 28

28

The Barn Swallow

FLIGHT SPEED AND MODE Barn Swallows skimming over a field in their pursuit of insects appear to fly very fast but that is deceptive. Their flight speed has been recorded in several ways: with a stopwatch, a Doppler radar handgun, from film of foraging birds, from radar tracking of migrants and in a wind tunnel. These measurements have given values of 4–19 m/s, usually 8–11 m/s when foraging. In Scotland, for example, the average speed of foraging Barn Swallows was 10.4 m/s with a range of 5.5–18.8 m/s (Waugh 1978; Turner 1980). For migrating Barn Swallows radar-tracking studies revealed average speeds of 11.5 and 12.8 m/s (Bruderer & Boldt 2001). In a wind tunnel, Barn Swallows were able to maintain flight down to 4 m/s and up to 14 m/s (Park et al. 2001a). Birds can use two basic modes of flight: flapping and gliding. Flapping uses up a lot more energy but is faster than gliding flight. Barn Swallows use mainly flapping flight and periods of gliding are usually short, just a few seconds, between bouts of flapping. In my study, on average they glided only 20% of the time they were foraging. This varied, though, from 39% early in the season to 7% when feeding second broods (Turner 1980). The variation may be caused partly by the birds having more ‘spare time’ before breeding and partly by differences in the weather and prey availability. Late in the season when the temperatures are high, faster flight may be needed because insects are more active then. In particular, fast flight is needed to catch strong-flying insects such as horse flies and bluebottles, and Barn Swallows fly fastest when hunting these insects (Turner 1980). Slower flight with more glides seems to be used when the birds are feeding on swarms of weak-flying aphids or midges. Speed also varies with height: Barn Swallows fly fast when chasing prey low over the ground and slowly at higher altitudes. Blake et al. (1990) recorded average speeds of 8.6 m/s for Barn Swallows foraging low down and 6.8 m/s for those above 0.5 m and flying erratically. At high altitudes, Barn Swallows may also fly slowly to watch out for prey (Warrick 1998). I found that temperature was the main factor determining which flight mode was used: Barn Swallows used more flapping flight in good weather than in bad weather (Turner 1980). Barn Swallows are more manoeuvrable at high speed, mainly because when they are flying upwards to catch an insect from below (which they do on about 60% of prey captures), they can turn within a smaller radius than at low speeds, and they can overtake the insect before it has time to escape (Warrick 1998). The reason Barn Swallows usually fly up to catch prey is perhaps to prevent it diving, a common escape response of insects; in addition, insects are likely to be easier to see against the sky than against vegetation. Studies of Barn Swallows in wind tunnels, and on migration observed with radar, have provided more detail about their distinctive flying style (Pennycuick et al. 2000; Bruderer et al. 2001; Park et al. 2001a; Liechti & Bruderer 2002). During long flights, many passerines have a regular wingbeat alternated with short periods in flight when they glide on extended wings or fold or half-fold the wings, thereby

14639.qxd

24/1/06

3:53 pm

Page 29

Flight and feeding behaviour

29

getting some rest. Barn Swallows, and other hirundines, are more flexible in the way they fly, varying how often they flap their wings and for how long each downstroke and upstroke of the wings lasts. The duration of downstrokes is shortest at high speeds and when the birds are climbing, and the amplitude of the wingbeat is largest with fast downstrokes. The wingspan also changes during flight, being smallest in the middle of the upstroke as the wings are drawn in towards the body, and largest in the middle of the downstroke as the wings are spread out; wingspan decreases at faster speeds, up to 10–11 m/s, especially during the upstroke. Reducing the wingspan probably increases lift while reducing drag (Park et al. 2001a). The variable nature of the Barn Swallow’s flight is largely the result of interrupted upstrokes of the wings when the birds flex their primaries and only partially spread their wings; this so-called ‘partial bounding’ increases at nearly level flight and high speeds and probably allows the birds finer control over the force generated during the stroke. This differs from gliding flight, where the wings are fully spread and where profile drag, as well as lift, increases. In the wind tunnel, gliding was seen only during steep descents (Bruderer et al. 2001). Their pattern of flight, with irregular flapping durations and often single wingbeats, gives hirundines a distinctive radar echo-signature. Because Barn Swallows fly during the day and low down, they are likely to encounter air turbulence, which other species on long flights, migrating at night and high up, avoid. However, varying their wingbeat pattern may help Barn Swallows to fly in turbulent air and may increase stability during foraging (Bruderer et al. 2001; Liechti & Bruderer 2002). The frequency of wingbeats increases with an increasing angle of flight, that is, flapping is faster when the bird climbs. Wind tunnel tests have also found a U-shaped relation between wingbeat frequency and speed, that is, faster flapping at both slow and high speeds (Bruderer et al. 2001; Park et al. 2001a), but this was not seen in free-flying migrating Barn Swallows, where angle of flight was of overriding importance (Liechti & Bruderer 2002). In the latter study, speed and flight angle were negatively correlated: Barn Swallows flew slowly, down to 5 m/s, when climbing, and descended rapidly along the flight path, up to 19 m/s. For free-flying migrating Barn Swallows, average wingbeat frequencies were 4.4 Hz overall, and 5.4 Hz during horizontal flight (range 2.5–8.4 Hz, Liechti & Bruderer 2002); and Danielsen (1988) recorded a wingbeat frequency of about 9 Hz. Warrick (1998) also recorded wingbeat frequencies of 14 Hz for free-flying Barn Swallows during acceleration, 9.9 Hz for those catching insects and 8.2 Hz for foraging birds. In wind tunnel studies, wingbeat frequencies were 6.1 Hz for juveniles (range 2.5–8.5 Hz, Bruderer et al. 2001) and 7–9 Hz for adults (Park et al. 2001a). However, differences between the studies, for example in the way wingbeat frequency was measured and the age and number of Barn Swallows involved, make it difficult to compare them. Wind tunnel tests with juveniles suggest that they have higher flight costs than one would expect from theory, but whether this is an effect found only in wind tunnels, or whether it applies to free-flying birds, is not clear (Pennycuick et al. 2000; Liechti & Bruderer 2002). With their short wingspan, juveniles may fly less efficiently than adults (e.g. Gatter & Behrndt 1985; Liechti & Bruderer 2002).

14639.qxd

24/1/06

3:53 pm

Page 30

30

The Barn Swallow

ADAPTATIONS FOR FLIGHT Compared with other birds of similar size, Barn Swallows, like other hirundines, use only about 60% as much energy during flight (Hails 1979; Turner 1983). In part, this is because some of their flying time is spent gliding, which does not use up much energy, but more importantly their shape also keeps costs down (Hails 1979). The long wings and low wing loading (the ratio of weight to wing area) may reduce the power that flying birds need to support their weight, generated by the wings pushing air downwards (induced power). The flying birds’ bodies create drag, and power is also needed to overcome this; however, the Barn Swallow’s streamlined shape, with a cone-shaped head, short neck and tapering abdomen and tail, reduces this ‘parasite power’. Wings also cause drag but this, and the ‘profile power’ needed to overcome it, is reduced by their high aspect ratio (long wingspan in relation to wing area). The high aspect ratio and the low wing loading also allow Barn Swallows to fly slowly when turning to catch insects. The wing shape thus makes Barn Swallows manoeuvrable and their flight very economical. The tail is used a great deal in flight; it is carried almost closed in straight flight but can be spread wide, raised, lowered or twisted as necessary when the bird slows or turns (Norberg 1994; Figure 2.1). The function of the bird’s tail from an aerodynamic perspective, however, is still poorly known (Hedenström 2002). It is usually thought of as a delta wing, similar to the wings of modern fighter aircraft and Concorde (Thomas 1993a, 1996a, b). The lift provided by the tail should be proportional to its maximum continuous span; drag created by the tail, in contrast, should be proportional to its surface area, so the best shape for a tail when fully spread is thought to be a triangle with straight trailing edges, in which case the outer feathers would ideally be twice the length of the central ones (Thomas & Balmford 1995). Male Barn Swallows, however, have outer feathers much longer than this, which would theoretically just increase drag (Evans & Thomas 1997). Norberg (1994) examined how Barn Swallows use the tail, by filming them and in wind tunnel experiments. He suggested that the streamers, which are the distal parts of the outermost feathers, control the attitude of the whole feather, so as to reduce drag and increase lift. When the birds spread and lower the tail, the drag on the streamers rotates the outer tail feathers to deflect the leading edges downwards, like the activation of vortex flaps on an aircraft wing. This would reduce drag and increase the amount of lift obtained from the tail, and so enable the birds to turn more tightly, which would increase foraging efficiency. The streamers may therefore have an aerodynamic function, at least in part, as wind tunnel experiments also suggest. These show that Barn Swallows furl the tail, parallel to the airflow, at speeds above about 7 m/s, reducing drag, whereas they spread the tail when flying slowly and turning; at low speeds the bird’s body also tilts up more and the tail forms a larger angle of attack to the direction of the airflow, probably increasing the ratio of lift to drag (Park et al. 2001a; Evans et al. 2002). However, wind tunnel experiments also show discrepancies with theoretical predictions, suggesting that the tail does not

14639.qxd

24/1/06

3:53 pm

Page 31

Flight and feeding behaviour

31

Figure 2.1. Drawing from a high-speed film of a Barn Swallow making a sharp left-hand turn to catch an insect. Consecutive images are 1/100 s apart; the entire manoeuvre took 110 ms. The tail is spread wide and lowered in the turn and the streamers are bent backwards and upwards, deflecting the tail’s leading edge downwards. The alulae are raised, acting as leading edge flaps of the wings. From Norberg 1994.

fit the delta-wing model when widely spread and at large angles of attack (Evans et al. 2002; Evans 2003). Barn Swallows are particularly good at turning in flight. Waugh (1978) calculated manoeuvrability indexes (outer tail length divided by weight) for the British

14639.qxd

24/1/06

3:53 pm

32

Page 32

The Barn Swallow

aerial-feeding birds. Barn Swallows, which take the largest prey, are the most manoeuvrable with an index of 4.91, whereas Common Swifts, which do not need to change direction much when chasing their small weak-flying prey, have an index of 1.84. Northern House Martins and Collared Sand Martins, which take mainly small prey, are intermediate with indexes of 3.12 and 4.06, respectively. Analysis of film of birds flying to and from the nest also shows that Barn Swallows can turn more tightly than Northern House Martins (Park et al. 2000). There are also adaptations in the muscles controlling the tail, to improve manoeuvrability (Moreno & Møller 1996). The muscle that depresses the tail (the depressor caudae) is long in the Barn Swallow, with deep fibres, which provides a mechanical advantage around the pelvic joint and greater force when the muscle contracts. Relatively short pubocaudalis internus and externus muscles, which depress and rotate the tail, shorten rapidly, allowing rapid tail movements. The Barn Swallow also lacks a tendon between the pubocaudalis externus and the caudoiliofemoralis muscle that Collared Sand Martins and Northern House Martins have, and this may also help lower and rotate its more deeply forked tail.

Male tail length The Barn Swallow’s tail, however, is not just used for flight; the long tail of the male also plays a role in courtship (Chapter 4). There has been, and still is, considerable debate about whether the male’s long tail evolved to improve manoeuvrability in flight (i.e. by natural selection) or to attract females (i.e. by sexual selection), or both. Long tails clearly do confer mating advantages on males, as well as being associated with better parasite resistance, immune function and survival. Anders Møller and his colleagues showed this in a series of studies involving elongating and shortening the tails of Barn Swallows, by cutting and adding or removing pieces of feather; for example, males given long tails were more successful at getting both mates and extra-pair copulations (Chapters 4, 5). Exactly how these substantial manipulations, of 20 mm, affect flight and what they reveal about the tail’s role in sexual selection, however, is controversial (e.g. Evans & Thomas 1997; Thomas & Rowe 1997; Evans 1998; Møller et al. 1998b; Barbosa & Møller 1999a; Buchanan & Evans 2000; Rowe et al. 2001). These manipulations could have a large effect on the aerodynamics of the tail and thus on flight performance, so the costs of short or long tails to males are not clear. There is evidence from such experiments that males incur costs by having long tails (Chapter 4) and such tails do not appear to be ideal for foraging, perhaps because of the associated increase in drag: males with elongated tails thus catch smaller, and more, insects per food bolus than short-tailed males, whereas tail shortening increases the size of prey caught (Møller 1989c; de Lope & Møller 1993b; Møller & de Lope 1994; Møller et al. 1995a). Catching smaller insects may reduce the rate at which long-tailed males get energy (Turner 1980). Whether males with elongated tails are unable to catch large, fast-flying insects or whether they change how and where they feed, or whether they change what they catch in response to

14639.qxd

24/1/06

3:53 pm

Page 33

Flight and feeding behaviour

33

changes in their mate’s chick-feeding behaviour, is not clear (e.g. Matyjasiak et al. 2000b; Nudds & Spencer 2004). Males have some adaptations to reduce any cost of having attractive long tails (Møller et al. 1995c; Møller 1996b). The tip of the outer tail feather in males is narrower than in females, perhaps to reduce drag, and greater symmetry of the tip may make the air flow more even. According to some scientists, the Norberg mechanism described above may itself be an adaptation to reduce the costs of long tails (e.g. Møller et al. 1998b; Barbosa & Møller 1999a). Males also have slightly longer wings, a slightly lower wing loading and greater aspect ratio than females, which will improve manoeuvrability and offset the costs of long tails to some extent. Wing length and wingspan increase with increasing tail length but more so in females than males, however, so the cost saving is greater for longer-tailed females than for longer-tailed males. In contrast, some experiments indicate that mainly natural selection (to improve manoeuvrability) may have shaped the Barn Swallow’s tail. Evans (1998) videorecorded the flight of males whose tails had been shortened or lengthened by 20 mm, in the basal portion of the feather or in the streamer, or in neither. He found that the costs of flying, measured as velocity, acceleration and rate of change of heading, were higher for males with shortened or lengthened tails relative to males whose tails had not been changed, suggesting the latter were the optimal length for flight. Tails shaped solely by sexual selection (to attract females) would be longer than this optimum and shortening them should have reduced flight costs. However, the difference in tail length between males and females may still be the result of sexual selection acting on the male’s tail (e.g. Hedenström 1995; Evans 1998; Møller et al. 1998b). Further experiments support the idea that both natural and sexual selection have been involved in the evolution of the Barn Swallow’s tail. Buchanan & Evans (2000) shortened the streamers of Barn Swallows by up to 20 mm, by trimming the feathers rather than by cutting them, and then filmed the birds to record how well they flew to and from their nest site. Aspects of the Barn Swallows’ flight such as speed and agility varied in a U-shaped or n-shaped fashion with the extent of the reduction in streamer length; a reduction of 7–15 mm improved flight, and hence reduced flight costs, the most. Similar results were found for Barn Swallows during mobbing flight (S. Allombert, unpubl. data, cited in Buchanan & Evans 2000). Similarly, Rowe et al. (2001) assessed the ability of Barn Swallows with experimentally reduced streamers to fly through a maze with strings suspended from the roof and found that birds with a reduction of about 12 mm negotiated it better than those with shorter or longer reductions. These experiments suggest that Barn Swallows’ tails, at least in Scotland where the studies were done, are about 10–12 mm longer than is aerodynamically optimal, probably as a result of sexual selection, although what caused the initial lengthening, improved manoeuvrability or females preferring slightly longer tails, is not clear. Rowe et al. (2001) estimated that about 20% of the males’ streamers is sexually selected, most being the result of natural selection for aerodynamic performance. The effect of a reduction in streamer lengths also depends on the initial lengths. For short-tailed birds, for example, the optimal speed with the least costs is

14639.qxd

24/1/06

34

3:53 pm

Page 34

The Barn Swallow

likely to be lower than for long-tailed males, and a reduction in streamer length may increase costs for the former while decreasing them for the latter. Tail lengths decrease at lower latitudes, however (Chapter 1), and it is likely that some populations have tails that are close to the optimal length for flight, with little effect of sexual selection. Thus, where temperatures are high and insects difficult to catch, tail lengths may be near to those required for efficient hunting, whereas in cooler areas with easier-to-catch prey, males may be freer to grow long tails as a sexual signal to attract females. Barbosa & Møller (1999b) calculated the costs of having long tails, in terms of the drag caused by the long tail and the power required for flight, in males of seven populations in Europe. They found that flight costs increased with latitude because of the longer tails in northern populations and thus were highest where insects are likely to be easiest to catch. They suggested that northern males are less constrained by foraging costs, allowing them to evolve relatively longer, and more aerodynamically costly, tails. Experimental manipulations of tail length have more effect on how many and what size of prey are caught in Spain, where Barn Swallows catch smaller and fewer prey per foraging trip anyway, than in Denmark, suggesting that naturally long tails would indeed be more costly at lower latitudes (Møller et al. 1995). Furthermore, in a study in southern Spain, shortening the tails of males by 21 mm appeared to make flight more costly (measured in terms of haematocrit levels, i.e. the proportion of red cells in the blood, which reflects metabolic activity) than shortening them by only 1 mm (Cuervo & de Ayala 2005). Thus the natural tail length of males in this population seems to be about, or perhaps only slightly longer than, the best length aerodynamically. In an attempt to see whether selection for improved flight performance initiated the elongation of tails in Barn Swallows, scientists have added streamers to the tails of hirundines that lack them. Adding streamers, even short ones, to Collared Sand Martins improved their ability to fly through a maze (Rowe et al. 2001) and adding them to Northern House Martins increased their manoeuvrability during trips to and from the nest (Park et al. 2000). Both martins hunt smaller, weaker-flying prey than Barn Swallows do and may not need to be more manoeuvrable, so would not benefit from having streamers. During level rather than slow turning flight, streamers are probably costly because they will increase drag. Indeed, Matyjasiak et al. (1999, 2000a) found that adding streamers to Collared Sand Martins actually reduced foraging success, in terms of the feeding rate to chicks and the size of insects caught. An elongation of the outer tail feathers might have been beneficial for the Barn Swallow’s streamerless ancestor by allowing it to turn quickly in pursuit of large prey (e.g. Park et al. 2000, 2001b). This might have opened up a new feeding niche and reduced competition with other aerial-feeding species. The streamers might then have become longer through sexual selection to attract females. Alternatively, sexual selection might have been important from the outset if only good-quality individuals could cope with the costs of having streamers and thus tail lengths reliably indicated to females the quality of the males (Matyjasiak et al. 2000a, b). Another possibility is that the outer feathers initially became narrower to form streamers without increasing in length, to improve manoeuvrability (Matyjasiak et al. 2004).

14639.qxd

24/1/06

3:53 pm

Page 35

Flight and feeding behaviour

35

Experiments on other hirundines are open to interpretation and have fuelled the debate about how much the Barn Swallow’s tail is due to selection for aerodynamic performance and how much is due to sexual selection, and which factors led to the initial lengthening of the streamerless tail of the ancestral hirundine (e.g. Cuervo 2000; Matyjasiak et al. 2000a, b; Buchanan & Evans 2001; Møller & Barbosa 2001; Park et al. 2001b). The evidence does suggest, however, that the streamers act both aerodynamically and as an ornament that is attractive to females, with the relative importance of each of these functions probably varying between populations. The lengths of streamers may also be constrained by breeding biology (Evans 2004). Females, and North American males, may need shorter tails than northern European males because they incubate (Chapter 7) and would damage long ones while doing so. There are, however, various arguments against this. Male Barn Swallows in southern populations in Europe and North Africa also have short tails but do not incubate, and incubating females and North American males can easily keep their tails safely outside the nest (Smith & Montgomerie 1992; Møller 1994a; Barbosa & Møller 1999a). In addition, other hirundine species such as the Redrumped Swallow have both enclosed nests and long tails, albeit with shorter and rounder-tipped streamers than the Barn Swallow. Nevertheless, the risk of damaging the tail against the nest or substrate during incubation may be an additional factor in the evolution of tail length in North American males. As well as its length, the symmetry of the tail also affects its aerodynamic performance (Thomas 1993b; Norberg 1994; Møller & Swaddle 1997). If one outer feather is longer than the other, the lift produced across the tail will not be even, and rolling and yawing forces are created; less lift is generated, turning ability is reduced, drag may increase and more power is required for flight. The problem caused by asymmetry will be greatest when the tail is spread during slow flight, and manoeuvring and asymmetry will be more costly for longer tails. Males with tails made asymmetric in experiments fly less well, at least in the short term, hitting more obstacles with their wings on their way through an aerial maze (Møller 1991d). Moreno & Møller (1996) found that the muscles controlling the outer tail feathers are also asymmetric and suggested that this may reduce the aerodynamic costs of asymmetries in the feathers. It is not clear whether birds with tail asymmetries do experience substantial flight costs (Møller & Swaddle 1997); they may be able to compensate over the long term (Cadée 2000). Males may have asymmetric tails because of problems during growth of the tails or because pieces of the tails break. Asymmetry that develops during feather growth is negatively related to tail length in males, so males may suffer from length-related but not asymmetry-related costs, or vice versa. However, males with long tails are good-quality males and may be able to bear the costs (Møller 1994d). On the other hand, long tails are more likely to break during the breeding season, which would make the tails asymmetric and reduce flight performance (Smith & Montgomerie 1991; Barbosa et al. 2003). Although developmental asymmetries cause little harm during the breeding season, broken tails may be a disadvantage during migration. After the breeding season, tail damage is frequently seen, in one South African

14639.qxd

24/1/06

3:53 pm

Page 36

36

The Barn Swallow

sample occurring in 90% of adult males and 85% of adult females (N. Cadée et al., unpubl. data in Barbosa et al. 2003). Tails can be damaged in a number of ways, possibly including brushing against objects during interactions with other individuals; some parasites such as feather lice also weaken tails. Feather lice do not seem to affect flight directly, but may make their hosts change their behaviour; for example Barn Swallows infested with many feather lice tend to use more flapping flight while foraging, perhaps in an attempt to increase foraging efficiency (Barbosa et al. 2002). Parasite-damaged tails may also be a liability on long-distance flights such as migration, as females with many holes in their feathers tend to arrive and lay late and have poor survival prospects (Pap et al. 2005).

Female tail length Females have shorter outer tail feathers than males, but longer ones than juveniles. The length of the female’s outer tail feathers in relation to the inner ones appears to be closer to aerodynamically optimal than are the male’s streamers (Thomas 1993a; Norberg 1994), and females do not suffer the same flying costs as males do (e.g. Saino et al. 1997c; Chapter 4). However, when Buchanan & Evans (2000) and Rowe et al. (2001) reduced the streamer length of females they found that flight performance varied with streamer length as it does with males, suggesting that females, at least in Scotland, have longer than optimal streamers. The female’s tail does not seem to have evolved as an ornament to attract mates; it does not clearly reflect her attractiveness to males, reproductive ability or how good a parent she is, especially in the Spanish population, and a male would not necessarily benefit by mating with a long-tailed female (Chapter 4). Rather, tail length is probably genetically correlated in males and females, so selection for long tails in males may result in females also having slightly longer tails than juveniles (Møller 1993c; Møller et al. 1998b). The length of the juvenile’s tail may be close to optimal for flight (Cuervo et al. 1996b; Park et al. 2001b).

DIET Barn Swallows feeding themselves rather than getting food for chicks take a variety of insects, but especially beetles, Hymenoptera (an order of insects that includes ants, bees, wasps, ichneumon wasps and sawflies) and flies (Table 2.1). Other invertebrates in the diet include aphids and other bugs, moths, mayflies and spiders. When available, swarming insects such as flying ants are caught in large numbers: Beal (1918) found over a thousand ants in one stomach. The type of insect taken varies during the season. In North America, flies formed 82% of the diet in March and only 18% in September (Beal 1918). Early in the season in Scotland, small flies also formed a high proportion of the diet of egg-laying and incubating adults (Turner 1982b).

14639.qxd

24/1/06

3:53 pm

Page 37

Flight and feeding behaviour Table 2.1.

37

Percentage composition of the diet of adult Barn Swallows in the breeding and non-breeding seasons.

Source

Location

% Beetles

% Hymenoptera

% Flies

Poland Crimea Scotland

14.4 39.8 26.1

78.0 42.8 1.0

1.9 12.8 69.1

Malawi South Africa Malaysia

36.8 56.9 6.0

48.3 12.5 82.0

7.6 3.4 8.0

Breeding season Glowacki 1977 Kostin 1983 Turner 1982b Non-breeding season Waugh 1978 Kopij 2000 Waugh & Hails 1983

Adult Barn Swallows also readily take grit such as pieces of eggshell or mollusc shell as an aid to digestion or as a source of calcium, especially females during egglaying (see below and e.g. Merrill 1976; Dhondt & Hochachka 2001; Oliver 2002). Beal (1918) found a small amount of plant food in the stomach contents he analysed, some of which might have been picked up as grit or taken accidentally along with insects from various substrates. Substantial quantities of plant food (elderberry and red osier dogwood) were found in one stomach and there are reports of Barn Swallows feeding on berries (von Vietinghoff-Riesch 1955). These seem to be taken early in the year and may be an alternative food when insects are not yet abundant, but their nutritional value to Barn Swallows is not known. They may be no more than a last resort when nothing else is available. However, Barn Swallows can digest some plant food, and do sometimes eat it when not breeding. In South Africa they eat the seeds of Acacia cyclops trees, taking them while either hovering briefly or perching. They digest the fleshy outer part, which is rich in protein, and regurgitate or egest the seed itself. From seeds present in the faeces of birds caught in January in the Cape, Hofmeyr (1989) estimated that 80% of the Barn Swallows present were eating them. This seems to be a recently acquired habit, as this tree has been introduced from Australia, and Barn Swallows may be helping to spread it (Hofmeyr 1989; Keith et al. 1992). In the winter habitats, the main prey are flying ants, beetles and flies (Table 2.1). Spiders, caddisflies, grasshoppers, termites, aphids and other bugs, butterflies and moths, and ichneumon wasps and other hymenopterans have also been recorded (e.g. Waugh 1978; Cramp 1988; Keith et al. 1992). Some non-flying prey items are taken when abundant; for example wintering Barn Swallows have been recorded hovering over vegetation to pick up bugs and caterpillars and catching sand-hoppers on a beach. When swarming after rain, termites can also be an important food source (van Ee 1988); van den Brink et al. (1997) noted that Barn Swallows at a roost were so ‘stuffed with termites . . . they couldn’t close the bill because of protruding

14639.qxd

24/1/06

38

3:53 pm

Page 38

The Barn Swallow

insects’. In Malaysia, the diet includes a high proportion of flying ants (46% of prey) and these become more important as a food source as migration time approaches (Waugh & Hails 1983). The relative lack of flies in the winter diet is striking, considering their importance during the breeding season (see below). The sheer abundance of ants when swarming may make them more profitable to catch (Waugh 1978), but Waugh & Hails (1983) also suggested that such slow-flying insects may be easier to capture than more mobile flies by birds whose flying ability is compromised by moulting tail feathers, accounting for the increase in ants taken before migration. Similarly, beetles may also be easier to catch than flies. Barn Swallows may also avoid competing with other aerial-feeders, especially those that are breeding, by concentrating on prey other than flies (Waugh 1978; Waugh & Hails 1983). In contrast, flies, particularly large ones such as horse flies and hover flies, are overwhelmingly the most important part of the chicks’ diet, making up 73% of items in Scotland and from 43% in a German study (Schulze-Hagen 1970) to 87% in eastern Siberia (Dragunkina 1986). Aphids and other bugs are also commonly fed to the chicks along with a few beetles, hymenopterans, butterflies and moths (adults and occasionally caterpillars), mayflies, damselflies, stoneflies, lacewings, caddisflies, scorpionflies, thrips, earwigs and spiders (Cramp 1988). The diet varies with the time of year, depending on which types of insect are most available. In my study, the main seasonal differences were an increase in aphids and a decrease in horse flies, hover flies and muscid flies (such as house flies and stable flies) in the diet over the summer (Turner 1980). Similarly, in Denmark, first broods were fed mainly flies whereas aphids were more important for second broods (Møller 1994a). In Germany, Loske (1992) found a change from mainly dance flies, muscid flies and mayflies in June to plant bugs, snipe flies and hover flies in July, and march flies and hover flies in August. In Switzerland, the main prey were brachyceran flies (such as horse flies and hover flies), but nematoceran flies (such as midges) were important in early September; calyptrate flies (such as blow flies) peaked in the diet in June and August, snipe flies in July and aphids and soldier flies in June and July (Egger 2000). The type of prey also depends on what is available locally. One pair of Barn Swallows in Scotland caught lots of mayflies from a river and another pair often hunted moths attracted to a light in the evening, whereas these were rare prey for other pairs. In addition to food, parent Barn Swallows give their chicks grit. This is probably a source of calcium, which the chicks require for bone development, and the harder particles may help to break up the tough exoskeleton of the prey. In an analysis of the stomach contents of chicks, Barrentine (1980) found that four out of five contained grit, mostly light-coloured 1–3 mm pieces. About a third of the pieces of grit, such as mollusc shells, contained calcium. Anders Møller (pers. comm.) noted Barn Swallows both eating chalk, which had fallen from the walls of farm buildings, and feeding it to chicks.

14639.qxd

24/1/06

3:53 pm

Page 39

Flight and feeding behaviour

39

SELECTION OF PREY When Barn Swallows collect insects for their chicks, they usually catch several before returning to the nest, keeping them packed into a ball or bolus in the throat. I recorded 1–126 insects in a single bolus but the average was only 18. Other studies have reported up to 175 insects in a bolus, with average numbers of 3.5 to 19. Smaller food boluses are collected for second broods than for first ones (Bryant & Turner 1982; Jones 1987b; Loske 1992). In Scotland, most prey items were larger than 5 mm (83% of first-brood prey, 72% of second-brood prey; Waugh 1978; Turner 1980). The range of prey size taken is mostly c. 1–23 mm, although some larger insects up to 50 mm are occasionally eaten (e.g. Waugh 1978; Kozena 1980; Loske 1992). The size of prey caught varies during the breeding season. Waugh (1978), Loske (1992) and Egger (2000), for example, reported that, on average, smaller insects such as aphids, March flies or nematoceran flies were taken later in the summer. In contrast, in my study, second broods were fed larger items on average than first broods (Turner 1980); however, these large items were mainly moths and crane flies, whereas fewer large brachyceran flies were fed to second broods (40.8% versus 58.1% for first broods). The size and number of insects in a bolus also vary geographically, probably because of differences in climate. In Spain’s warm climate, for example, where large insects are likely to be more active and difficult to catch, male Barn Swallows take more small items than in Denmark (average length 7.5 mm in Spain versus 10.8 mm in Denmark), and catch fewer per foraging trip (11.4 versus 15.5) (Møller et al. 1995a). Parents bring larger items back to the nest than they eat themselves and eat smaller items when they have chicks than beforehand; in winter in Africa, however, Barn Swallows catch larger, but less mobile, insects than when breeding (Waugh 1978). In my study, the prey taken by adults weighed 10 mg on average, significantly less than that fed to chicks (22 mg). In addition, the larger the prey available at a feeding site, and the further away from the nest it is, the larger the prey caught by the parents (Waugh 1978). These differences are probably the result of the extra effort of travelling to and from the nest when feeding chicks: to make the trip worthwhile the adults take back large insects, especially bulky flies, whereas when feeding themselves they can profitably feed on smaller insects. The types of insects caught are diverse taxonomically: Kozena (1979), for example, recorded over 80 families of insects in the diet. However, Barn Swallows do not just take any insect they come across. Rather, they prefer to hunt large, active ones and these are typically large flies. These preferred insects are also often found alone rather than in swarms. Large mobile insects take more energy to catch than small weak-flying ones do because they require faster pursuit with flapping flight and fewer can be caught per minute, but they provide a lot more energy so are more profitable to hunt (Turner 1980). Their capture also requires a high degree of manoeuvrability and the Barn Swallow’s wings and tail are well suited for this purpose. In addition, the Barn Swallow’s bill is adapted to snatch these large insects, as

14639.qxd

24/1/06

40

3:53 pm

Page 40

The Barn Swallow

it has a large cross-sectional area; the bills of aerial-feeding birds that catch small prey are narrower (Waugh 1978). Barn Swallows catch more large insects and fewer small ones than are available in the environment. Of the main groups of flies, Barn Swallows in Scotland particularly selected horse flies, hover flies, blow flies and muscid flies: these groups made up higher proportions of the diet than in samples of flying insects that I caught with a sweep net in the same places, whereas there were relatively fewer crane flies, dung flies and large hymenopterans in the diet than were available (Turner 1980). Flies in the diet were also among the largest found in the environment, but the very largest, fastest flies were selected less than expected (Turner 1980). I also found that late in the summer, when these large flies became more abundant, Barn Swallows shifted their choice towards medium-sized flies (Turner 1980). The most frequent size of large, fast-flying flies taken in Waugh’s (1978) study was 7–11 mm. Fewer larger flies were caught suggesting that they may take too much energy or time to catch and are therefore not profitable prey. This would be so particularly at high temperatures when insects are more active and large, fast-flying species are more difficult to catch. In contrast, much larger flies than this were caught when they were slow-flying ones such as crane flies (most frequently up to 21 mm long). Waugh suggested that the mobility of the prey, rather than size, determines whether it is included in the diet. Even when large insects are not very abundant, Barn Swallows will seek them out, and as large insects increase in abundance, proportionately more are brought back to the chicks; in contrast, small insects are often ignored, regardless of how abundant they are (Waugh 1978; Turner 1980). Small insects are still caught, however, particularly when they are relatively abundant, and boluses can contain a mixture of insects of various sizes. Indeed more small prey are taken than expected from theoretical predictions of the optimal selection of prey by a predator (Turner 1982a), perhaps because as the bird’s throat becomes filled up with insects, it may take longer to manipulate the catch, so it may become more profitable for the bird to catch small insects (Houston 1985). Some insects may be difficult for the parents to manipulate; large active insects attempt to struggle free when passed to the chicks, whereas small insects are packed into a cohesive ball. Noctuid moths, such as the antler moth, which the Barn Swallows in Scotland often caught late in the summer in bad weather, were particularly prone to escaping (Turner 1980; Bryant & Turner 1982). Although bees are sometimes taken, these are often drones, rather than the workers which sting (Kozena 1979; Turner 1980). Bees may be useful prey early in the morning, however, as they are active at lower temperatures than large flies. They may also occasionally be an abundant source of food; Wilde (1992), for example, noted Barn Swallows feeding in the flight line between a hive and the bees’ feeding site and collecting several of the bees for their chicks. Wasps are also rarely taken (e.g. Gabriel 1975), although hover flies, which mimic wasps, are. In my study, bees and wasps made up less than 1% of the diet. Few types of insects are avoided, although in Scotland dung flies were not often taken. Dragonflies are also rare in the diet, perhaps because they are very fast and difficult to catch and they are also rather large for a chick to swallow.

14639.qxd

24/1/06

3:53 pm

Page 41

Flight and feeding behaviour

41

FEEDING SITES AND THE EFFECTS OF THE WEATHER Barn Swallows hunt close to their nest site when this is possible, and the feeding range of one pair may overlap with those of other pairs, from both the same and other breeding groups. In Scotland, Barn Swallows fed on average 170 m, and up to 600 m, from the nest, in Møller’s (1987d) study up to 500 m from the group (median 100 m), and in Italian and North American populations mostly up to 400 m (Snapp 1976; Ambrosini et al. 2002a). Similarly, in mixed farmland in Oxfordshire, England, fields within 300 m of a nest site, compared to those 300–600 m from the nest, contained a greater number of foraging Barn Swallows, which also foraged for longer in the closer fields (Evans 2001). In Switzerland, a study with four radiotagged Barn Swallows found that they foraged mostly within 500 m of the nest and covered a range of 8–9 hectares (Swiss Ornithological Institute, M. Grüebler, B. Naef-Daenzer & L. Schifferli, pers. comm.). Distance from the nest site appears to be more important than prey abundance in determining where Swallows forage, perhaps because travelling to distant sites is too costly in terms of energy use (Waugh 1978; K. Evans, R. Bradbury & J. Wilson, unpubl. data). Since Barn Swallows do not travel far to hunt, the area around the nest site needs to have one or, preferably, more good sources of flying insects, such as waterbodies, pastures with livestock, manure heaps, and shelterbelts or woodland edge. The habitat also needs to be open to allow for aerial pursuit of prey, so woodland itself is not suitable. In farmland, Barn Swallows do forage over crops such as cereals and rape, particularly flowering rape (Watson & Rae 1998), but other habitats are clearly preferred. For example, in an Italian study, Barn Swallows were seen foraging over hayfields 13 times as much as over maize fields (Ambrosini et al. 2002a). Grazed fields are an excellent source of insects, providing more and a greater variety of types of insect than silage and cereal fields, and, in consequence, Barn Swallows forage over grazed fields more than they do over silage, arable or set-aside fields (K. Evans, R. Bradbury & J. Wilson, unpubl. data; see also Chapter 6 and BTO News, Nov–Dec 2005, pp. 24–25). Livestock, and manure heaps, around the farmyard also provide a source of insects close to the nest (Loske 1994). Hedgerows are a better source of insects than are fields, especially arable compared with grazed fields (Morand 2000; Evans 2001), and Barn Swallows use hedgerows more in arable habitat than when they can feed over grassland (Evans 2001; Evans et al. 2003a). Field boundaries with trees, which provide an additional source of insects, are also preferred to those without (Evans 2001; Evans et al. 2003a). As well as providing more insects, hedgerows may also reduce the energy costs of flight because of the lower wind speeds and warmer temperatures associated with them (Evans et al. 2003a). However, predators such as Eurasian Sparrowhawks may use hedgerows as cover while hunting, and Barn Swallows may therefore avoid them if insects are available elsewhere. Insects are a patchy food source, their abundance often varying both between sites and over time. So Barn Swallows often have to change their feeding sites to exploit the best patches of insects. For example, insect numbers vary over the breeding

14639.qxd

24/1/06

42

3:53 pm

Page 42

The Barn Swallow

season; in Scotland they increased in the spring and then fluctuated over the summer, depending on the weather (Waugh 1978; Turner 1980). The amount (biomass) of insects available also increased during the day, peaking mid-afternoon in Scotland, because of an increase in large insects: large flies are most active at and after midday, when temperatures are high (Lewis & Taylor 1965; Waugh 1978). This daily increase in availability of large insects, and the average size of insects, was also greater late in the season in Scotland when second broods were being reared. Seasonal changes in abundance vary geographically, however; for example, larger insects were scarcer late in the breeding season in a study in southern Spain (J.J. Cuervo & A.P. Møller, unpubl. data). Different feeding sites are used at different times of the season, depending both on this variation in the availability of insects and on the stage of the nesting cycle; Barn Swallows may travel further, for example, at times when they do not have to return to the nest frequently to incubate eggs or feed chicks. Loske (1992) recorded Barn Swallows using areas of water especially in April, May and September, forest edge, hedges, oak trees and dung piles in June and July, and lime trees, parkland and lawns in August; this led to a change in distance travelled from the nest to a feeding site from 812 m on average in June to 237 m in August. I also found a decrease in average distance travelled during the season from 295 m during nest-building and 312 m during egg-laying to 269 m during incubation, 188 m while feeding the first brood and 138 m for the second (Turner 1980). A major cause of variation in food availability is the weather, which has a profound effect on insects (e.g. Taylor 1963; Peng et al. 1992; Blackwell 1997). Large flies are more active and can escape capture more easily at high temperatures and may not fly at all at low temperatures. Small, weak-flying insects, in contrast, are less affected by temperature, but are subject more to the vagaries of the wind, which can create localised aggregations of insects that are blown to, or seek out, a sheltered spot. Rain also reduces insect activity. Insects can be two or three times as abundant in fine weather as in cool, wet or windy weather. Consequently, where and how successfully Barn Swallows feed also depends on the weather. Waterbodies and shelterbelts such as hedgerows and trees are the main places where Barn Swallows might find food in adverse weather. Even then, however, in cool weather they are likely to find only relatively small insects such as midges. In a study in England, during bad weather Barn Swallows preferred to feed along hedgerows, where insects were more abundant, rather than over the centre of fields; 95% of observed foraging time was spent in the former habitat compared with 26% in good weather (Evans et al. 2003a; Figure 2.2). Similarly, in bad weather, Swiss Barn Swallows also used hedges, where there were twice as many insects as over fields (Morand 2000), as well as trees and water; in addition they hunted around cattle and their dung, in pastures and near stables (Egger 2000; Swiss Ornithological Institute, L. Schifferli & M. Grüebler, pers. comm.; Figure 2.3). In bad weather conditions, Barn Swallows often have to go further from the nest to localised feeding sites (Bryant & Turner 1982), although a farm with livestock may still have insects around the farmyard (Loske 1994). For example, in Scotland

14639.qxd

24/1/06

3:53 pm

Page 43

Flight and feeding behaviour

43

Figure 2.2. The proportional use of vegetated field boundaries, compared to their area, by foraging Barn Swallows in good and bad weather. Hedgerows are preferred to field centres in bad weather. Vertical lines represent standard errors. From Evans et al. 2003a.

the distance averaged 148 m when the temperature was 20°C or more and 203 m when it was 16 °C or less (Turner 1980). Radio-tagged Barn Swallows in Switzerland fed within about 200 m of their nest, in a generally dispersed manner, in good weather, but in bad weather they tended to concentrate at certain sites such as hedgerows and waterbodies, which were sometimes more than twice as far away (M. Grüebler, pers. comm.; Figure 2.3). The weather affects not only the location of feeding sites but also the type and size of insect caught, the size of each meal brought to the chicks and how long it takes to collect. Both large, active insects such as horse flies and small, weak-flying, swarming ones such as aphids contribute to an abundant food supply and hunting Barn Swallows take both. In bad weather, in contrast, fewer types of insects may be available. For example, on one day of very bad weather in Scotland, Waugh (1978) found that midges comprised 82% of the diet of adult Barn Swallows, mosquitoes 2% and mayflies 6%, with a few other small flies, beetles and aphids making up the rest. Studies of the chicks’ diet in Scotland and Switzerland showed that in good weather parents caught mainly brachyceran flies, whereas in bad weather they caught many more nematoceran flies and plant bugs, but fewer brachyceran flies, especially hover flies and horse flies, and other insects (Table 2.2). The Swiss Barn Swallows also caught more mayflies, associated with waterbodies, and more flies associated with dung and cattle (sepsid flies, the drosophilid fly Drosophila repleta, dung flies and stable flies) than they did in good weather (Egger 2000; Swiss Ornithological Institute, L. Schifferli & M. Grüebler, pers. comm.). In addition, insects caught in good weather were larger (averaging 7.4 mm) than in bad weather (4.9 mm) (Egger

14639.qxd

24/1/06

3:53 pm

44

Page 44

The Barn Swallow (a)

(b)

Figure 2.3. (a) Insects are more abundant in sunny weather (dark grey) than in wind and rain (light grey); in bad weather, insects are twice as abundant around water bodies, barns and hedges as in fields. (b) Habitat use of radio-tagged Barn Swallows in Switzerland in good and bad weather. The nest is indicated by a star. The continuous black line around the nest shows the main feeding area in warm, sunny weather. The small circles show the feeding sites used on cool days (trees and hedges, indicated by black lines and the arrow). Dark grey: grassland; light grey: arable. From Kohli et al. 2004.

2000). In Scotland, I found that food boluses were largest in warm, dry conditions and these contained a high proportion of large flies, many consisting of just a few horse flies and hover flies, but also some small insects (Turner 1980; Bryant & Turner 1982). In poor weather, boluses typically contained few large flies and dozens of small ones. In Germany, boluses collected in wet weather were large and included lots of mayflies, snipe flies and muscid flies (Loske 1992). On average a meal in Scotland was collected in 2.4 minutes, but this depended greatly on the availability of insects. In good feeding conditions, Barn Swallows

14639.qxd

24/1/06

3:53 pm

Page 45

Flight and feeding behaviour Table 2.2.

45

Percentage composition of the diet of Barn Swallow chicks in good and bad weather.

Prey (%)

Scotland Good weather

Scotland Bad weather

Switzerland Good weather

Switzerland Bad weather

Brachyceran flies Calyptrata (e.g. Blow flies) Syrphidae (Hover flies) Tabanidae (Horse flies) Nematoceran flies Homoptera (e.g. aphids) Ephemeroptera (Mayflies) Coleoptera (Beetles) Hymenoptera Others Sample size (no. of items)

69.8 27.9 12.4 4.4 12.3 2.6 1.4 1.2 1.0 11.7 3156

32.0 16.0 1.9 0.1 21.0 41.5 0.9 0.7 0.9 3.0 1804

66.1 17.3 10.4 18.8 11.2 5.2 0 6.8 8.9 1.7 1516

45.3 12.4 3.0 0.9 22.8 13.3 10.7 2.7 3.5 1.9 516

Scottish data from A. Turner, unpubl. data and Swiss data from Swiss Ornithological Institute, B. Egger, L. Schifferli & M. Grüebler, pers. comm. Good weather: Scotland, 16°C or more, little or no wind or rain; Switzerland, 18 °C or more, sunny, little cloud cover; bad weather: Scotland, 15°C or less, with or without rain or strong wind, or 12 °C or less without rain or wind; Switzerland, less than 18°C, rain or 80–100% cloud cover.

would take under two minutes on average, sometimes just 30 seconds, but in poor conditions nearer six minutes. In terms of energy, Barn Swallows in my study collected 36 kJ per hour on average for the chicks, but could collect an average of 43 kJ per hour in good weather and only 15 kJ per hour in cool or wet weather. Foraging times clearly depend on the distance the Barn Swallows have to go to find food, so the presence near the nest of sites such as hedges with trees, which provide a source of insects in poor weather, is important for maximising the amount of food brought to the chicks. Insect availability also varies with height above ground, insect populations generally being more numerous, more stable and at higher densities near ground level. Morand (2000) found that insects were seven times less abundant at 7–8 m above ground than at ground level. Size also varies in this way, larger insects being concentrated low down (Waugh 1978). Barn Swallows thus concentrate their feeding low down over open ground or water in the breeding season. Waugh (1978) recorded Barn Swallows foraging at a mean height of about 7 m throughout the breeding season and Evans (2001) reported that Barn Swallows feeding chicks flew at an average height of about 1.1–1.3 m; Barn Swallows also feed lower in good weather than in bad (Turner 1980). They feed in similar sites in their winter quarters in Africa, although the lack of low temperatures and of high wind speeds means that Barn Swallows there use shelterbelts rather less (Waugh 1978). In Malaysia, Waugh & Hails (1983) found that Barn Swallows fed at lower levels and away from vegetation when temperatures were high, and near to vegetation in windy weather.

14639.qxd

24/1/06

3:53 pm

Page 46

46

The Barn Swallow

FEEDING TECHNIQUES Barn Swallows are usually seen sweeping to and fro across a field or river, chasing flying insects; but they are particularly attracted to places where insects are concentrated, for example midges in a mating swarm or mayflies emerging on a river, or, in Africa, flying ants or termites (Cramp 1988). Other animals are often good sources of insects, both because they and their dung attract flies and because they flush out insects from the vegetation as they walk. Cattle, horses, humans, herds of game animals in Africa and flocks of birds such as starlings all serve this purpose. Humans provide additional sources of insects such as tractors ploughing fields, mowers cutting grass, and bright lamps that attract moths and beetles. Insects buzzing around a light can attract Barn Swallows well after daylight has faded (e.g. Knox 1992). Grass fires also provide a supply of insects fleeing the blaze, although Barn Swallows are not attracted to them as much as other hirundines are. Barn Swallows also occasionally perch on trees and other plants or on walls and walk on the ground to catch non-flying adult insects and caterpillars or sandhoppers, sometimes dead or dying ones (Cramp 1988). There are even records of them perching on a pig’s back, by a spider’s web and on a dunghill to get insects (Cramp 1988; Jacob 1998). They are clearly not built to chase prey adeptly in such circumstances, so perching and walking are reserved for times when the weather is bad and there are consequently few insects flying anyway or when there is an abundant source of easy-to-catch prey such as sand-hoppers on a beach or caterpillars on a tree. Sometimes, though, a perch is just used as a base from which to hawk for insects like a flycatcher. Barn Swallows also often hover or fly slowly to pluck prey from a substrate such as the ground, water, vegetation, manure heaps, buildings or around a light, sometimes combining this with settling for a few seconds. In this way they can take prey items such as moths or flies on a wall, caterpillars on a tree or emerging stoneflies or waterbugs at the water’s surface. Barn Swallows flying close to, or momentarily touching or perching on, vegetation, for example, may even flush insects themselves (Turner 1981; Rezanov 2003). There are also a few observations of Barn Swallows flying over water plucking small fish from the surface (Merzlikin 2001). Finally, Barn Swallows are not above stealing prey; one was seen to take a butterfly from a sparrow (von Vietinghoff-Riesch 1955).

14639.qxd

24/1/06

3:54 pm

Page p1

14639.qxd

24/1/06

3:54 pm

Page p2

14639.qxd

24/1/06

3:54 pm

Page p3

14639.qxd

24/1/06

3:54 pm

Page p4

14639.qxd

24/1/06

3:54 pm

Page p5

14639.qxd

24/1/06

3:54 pm

Page p6

14639.qxd

24/1/06

3:54 pm

Page p7

14639.qxd

24/1/06

3:54 pm

Page p8

14639.qxd

24/1/06

3:53 pm

Page 47

CHAPTER 3

Social behaviour and vocalisations The first sun rays appeared over the mountains of Urundi. The twittering and the rattling increased to a crescendo. A few minutes later the reeds exploded into a cloud of swallows. They rose like helicopters straight up about ten metres or so, then spread out like an umbrella . . . Kai Curry-Lindahl, 1953

Barn Swallows do many things in groups, especially gathering in large flocks and roosts outside the breeding season. They often preen, sunbathe, mob predators or just loaf around together, and males sing and display communally during the breeding season. Large flocks of non-breeding birds also congregate at rich sources of food such as termite swarms. However, historical evidence of natural group sizes and aspects of the Barn Swallow’s behaviour, such as the lack of parental recognition of

14639.qxd

24/1/06

3:53 pm

Page 48

48

The Barn Swallow

offspring, also suggest that this species does not traditionally nest in large groups. Nevertheless, Barn Swallows clearly often aggregate to breed and why they do this has been the subject of much research.

ROOSTS In the breeding season, females roost on the nest and their partners perch nearby, but communal roosts are also used in some circumstances. Early in the season, before territories are set up, Barn Swallows will form roosts away from the breeding sites in very cold weather (R.J.S. Safran, pers. comm.). In addition, unmated males will leave the breeding group after the first-brood period and both single- and double-brooded pairs often leave once they have completed breeding, although some birds will continue to feed at the site and roost near their nest or in another building for a few days or even weeks without attempting another brood (Thompson 1992; Møller 1994a). Fledglings also roost in or near their nest for a week or more (Chapter 8). Older juveniles, non-breeding individuals and those that have finished breeding roost communally, usually in reedbeds, tall grass, maize, willows, other trees or tall vegetation, especially in or near water, or on cliffs (Cramp 1988). Collared Sand Martin burrows may also be used (Mead & Pepler 1975). Roosts in the breeding season are usually smaller than those that develop in the autumn and winter, with up to a few hundred birds. In cold weather, at any time of year, Barn Swallows will also roost communally in buildings, often huddling together in rows or clusters to keep warm, even piling on top of one another. Nests of their own and other species are used in cold weather as well: von VietinghoffRiesch (1955) reported the discovery of 21 individuals in a Northern House Martin’s nest. In autumn and winter, Barn Swallows typically roost in reedbeds or other wetland vegetation, or in tall grasses or thickets; tall crops such as sugar cane or maize are also increasingly popular (e.g. Cramp 1988; Loske 1990a; Ford & Elphick 1993; BTO Swallow Roost Project Newsletter 2004) and trees are sometimes used (e.g. Nuttall 1998; van den Brink et al. 2003). Roosts can contain large numbers, often tens or hundreds of thousands, and sometimes even millions in the wintering areas (Keith et al. 1992; van den Brink 1997; A.P. Møller, pers. comm.). Roost size, however, depends on the local climate and can vary from year to year. At a site on the River Boteti in Botswana, for example, there were about 100,000 Barn Swallows in January 1993 when the river was high and reedbeds extensive, but two to three million in 1994 when the river was low and few reedbed roost sites were available. In contrast, in Ghana, roosting Barn Swallows were distributed in small numbers over several roosts (van den Brink et al. 1998, 2000). Trees are used infrequently and by small numbers, probably because they are more exposed to predators than wetland roosts are, but one roost of one to two million Barn Swallows in 34 Acacia trees is known in Botswana (van den Brink et al. 2003).

14639.qxd

24/1/06

3:53 pm

Page 49

Social behaviour and vocalisations

49

Sites in towns are sometimes used as roosts, notably in India, Malaysia and Thailand (George 1965; Medway 1973; Ewins et al. 1991). Here Barn Swallows roost on overhead wires or on trees and ledges of buildings, apparently oblivious of human traffic. A roost has been present in Bangkok, for example, since at least the 1960s and in 1987/1988 contained at least 280,000 individuals (Ewins et al. 1991). Towns probably provide a warm place for roosting, and Barn Swallows may also benefit from feeding on insects attracted to the lights (Ewins et al. 1991). An exceptional roost site was a ship in the Mediterranean, on which dozens of Barn Swallows roosted along a picture rail in the bar one night (Boyle 1995). Barn Swallows may gather at a roost an hour or more before sunset, at first flying rather aimlessly, but as dusk approaches they form tighter flocks and wheel rapidly over the roost site before dropping vertically in small groups and settling in the vegetation. They often continue entering the roost after sunset. They twitter while in flight and for several minutes after settling (e.g. Loske 1984; Cramp 1988). Within the roost, there is some shifting of positions: juveniles arrive early but may be displaced by older birds (Cramp 1988). They leave at about sunrise, often in several waves. The synchronous behaviour, large numbers, fast flight and habit of flying high before entering the roost and after leaving it probably make it difficult for raptors to catch individuals (Bijlsma & van den Brink, in press). The timing of roosting can be affected by the weather; in one case Barn Swallows were observed roosting during a late afternoon thunderstorm and leaving the roost once it had passed (Grobler & Nuttall 1999). Van den Brink et al. (2003) also noted that Barn Swallows entered a tree roost later in the evening than those in reedbeds, taking up positions on the uppermost, presumably safer, branches first. Roost composition in the breeding areas changes during the year, from a high proportion of adults in summer to more juveniles as the season progresses, when recent fledglings join and the older birds leave (Cramp 1988). By October a roost may contain only juveniles. Among the adults at a roost, males tend to predominate, as unmated males leave the breeding sites early. The majority of individuals in large wintering roosts also tend to be juveniles; but, as during the breeding season, the proportion of juveniles may increase during the season and approach 100% by the time older birds have started to return to the breeding grounds (Cramp 1988; van den Brink et al. 1998). Females and males are found in similar proportions (e.g. Broekhuysen & Brown 1963; Dowsett 1966; Møller et al. 1995b). Barn Swallows also sometimes roost with other species such as Collared Sand Martins and European Starlings. Barn Swallows feed over a large area around the roost, but mostly within a radius of 50 km (Cramp 1988; Ewins et al. 1991; Oatley 2000; Mead 2002). There is evidence of Barn Swallows using the same roost over an extended period. Nuttall (2003), for example, reported individuals being recaught at a winter roost, in three cases 34, 36 and 40 days after initially being ringed. However, wintering Barn Swallows also change roosts locally (Oatley 2000; van den Brink et al. 2003). How often they do so is unknown but it is likely that changes in feeding conditions force them to move to roosts where insects are more abundant; for example, Barn Swallows deserted a tree roost in Botswana after a drought (van den Brink et al.

14639.qxd

24/1/06

3:53 pm

Page 50

50

The Barn Swallow

2003). Longer movements during the non-breeding season are also known; for example, three Barn Swallows in southern Africa moved 433, 619 and 1,249 km, respectively (Oatley 2000).

COMFORT BEHAVIOUR In hot weather, Barn Swallows sometimes seek the shade of buildings or vegetation but they also often sun themselves, especially in the morning on the roof of the nest site, and this is usually a group activity. A typical posture is to lie with the body touching the surface, wings and tail outspread and body feathers raised. Individuals may bask for several minutes at a time, even on hot surfaces in direct sunlight. Blem & Blem (1992) recorded Barn Swallows sunbathing on roofs whose temperature was 47–56 °C at times when the air temperature was also high at 30–36°C; the birds were gaping with extended tongues by the time they finished the basking session. Why Barn Swallows sunbathe is not clear, but it may help to dislodge or kill ectoparasites (Blem & Blem 1992, 1993). Groups of Barn Swallows on wires are often seen engaged in some aspect of feather care. They spend some time each day preening, usually running the bill through the feathers, especially the wings and tail. They also scratch difficult-to-reach areas, such as the head and neck, with a foot raised over a wing. Scratching with the foot under the wing is rarer but is the method used if the bird is in flight (Burtt et al. 1988). Secretions from the uropygial gland, which help maintain the feathers, are occasionally used (on 3% of preening bouts; Møller 1991g). Preening is most frequent in the early morning and evening, before and after the birds set out to forage. It is done in bouts of up to a minute or two; at the end of a bout the bird often shivers. Individuals vary in how much preening they do, but spend up to 15% of their time doing it, with males preening more than females; partners have similar preening rates, however (Møller 1991g). Males may preen more because the number of parasites they have affects how attractive they are to females (Chapter 4) or because they acquire more parasites than females by promiscuous mating and fighting (Møller 1991g). Preening decreases during the breeding season, although individuals that preen a lot continue to do so (Møller 1991g). Barn Swallows usually bathe by plunging into water, sometimes repeatedly, but will also use other suitable material such as dust, smoke, cinders, mud, dew on grass and spray from waterfalls (Cramp 1988).

AGGRESSIVE BEHAVIOUR In spite of doing things in groups, Barn Swallows are not usually tolerant of close contact with other individuals. When perched, they keep their distance from each

14639.qxd

24/1/06

3:53 pm

Page 51

Social behaviour and vocalisations

51

other, coming together only in very cold weather. Hutton (1978), for example, found that North American Barn Swallows perch an average of 12 cm apart and increase this distance when preening, to give themselves more space. Disputes can arise over perching spaces with individuals gaping at, pecking and chasing each other. Aggression is shown by bill gaping and pecking, and submission by one bird directing its bill away from the other one. Young individuals, which may beg for food, are tolerated more than adults. Chases are frequently seen: pairs chase intruders at the nest and rival males chase each other, sometimes uttering alarm calls. Males will also engage in singing contests, perched side by side with carpal joints raised and feathers sleeked. Disputes sometimes lead to physical fights, mainly between males but also between females, and can last on and off for hours or days. Combatants sometimes entangle their feet and fall to the ground; some fights have ended in a bird being killed (Cramp 1988). In addition, birds fighting on the ground are vulnerable to predation by cats (Møller 1994a). Disputes, including fights, also arise over the possession of feathers when females are collecting them for the lining of the nest (e.g. Møller 1991c). Barn Swallows are aggressive to nest competitors of other species such as House Sparrows and Northern House Martins, in one instance drawing blood from a Black Redstart (von Vietinghoff-Riesch 1955). Barn Swallows actively mob and chase a variety of birds, both individually and as a group (von Vietinghoff-Riesch 1955; Cramp 1988; Brown & Brown 1999a). They will flock together to circle and mob predators by diving at them and uttering alarm calls, even when these are not a direct threat. When the predator moves off, the birds may continue to mob it. (See Chapter 8 for mobbing behaviour at nest sites.) They will also harass other birds such as waders, herons, kingfishers and pigeons, which may be mistaken for predators (although a Grey Heron has been observed capturing a hirundine, so may pose a rare threat, Keighley & Hall 1995), and bats which may be feeding competitors (Rosair 1975; Gossip 1995). Almost any species that approaches nests with young may be mobbed, whether a potential predator or not. A direct attack by a raptor, though, can cause Barn Swallows to scatter, uttering alarm calls, and they may either land on the ground or climb upwards to avoid it.

BREEDING DISPERSION Barn Swallows breed both solitarily and in groups. However, although Barn Swallows often breed in groups, they do not build nests adjacent to each other as truly colonial hirundines such as Cliff Swallows will do. Hence, Barn Swallows are often termed ‘semi-colonial’. The nests are usually built well away from each other; in Scotland they were often in separate buildings or, if two pairs were present, at opposite ends of a barn. In Møller’s Danish study (Møller 1983, 1987d), nests were an average of 4 m apart and in an Italian study (Brichetti & Caffi 1992) 5 m apart. In North America, nests on bridges were spaced at 3 m intervals (Jackson &

14639.qxd

24/1/06

52

3:53 pm

Page 52

The Barn Swallow

Burchfield 1975) and in culverts at 3.7 m intervals (Grzybowski 1979). In years when the population density is high, however, nests can be as close as 10–20 cm to each other (Møller 1983, 1991e; Saino et al. 1998; Brown & Brown 1999a). Medvin & Beecher (1986) recorded an average of 2.4 nests/m2 in groups of 40–50 under bridges in Ellensburg, Washington, in contrast to 0.1/m2 for groups of 2–18 on the outside of buildings in Seattle. Brown & Brown (1996) found that nests were dispersed uniformly at a culvert breeding site, rather than being clumped as Cliff Swallow nests were. Because the nests are open cups, pairs are not protected from the attentions of other birds and so can be hostile towards intruders. Nests may be closer together, however, if they are placed where the neighbours are not in constant visual contact, and buildings with beams and cross girders may thus encourage large numbers to nest there (e.g. Ribault 1982; Meier 2001). At a natural site on a rocky river bank, nests were close together (0.2–2 m) but at different heights, so again the birds could avoid seeing each other (Nikolaev 1998). Each pair defends a nest and a small space around the nest against other Barn Swallows, both neighbours and other intruders, although they have a common feeding area. The nest territory area covers about 4–25 m2 (Cramp 1988) and is used for breeding, roosting and some preening. It can include a second old nest, which is sometimes used for second broods (Chapter 6). Barn Swallows may catch a few flies near the nest but usually feed outside their territory. The size of the defended area varies during the breeding season, from an average of 7–8 m2 before incubation to about 4 m2 during it, as males will attack conspecifics further from the nest before the eggs are laid (for both first and second clutches), presumably because of the greater risk of being cuckolded then (Møller 1990e; Chapter 5). As a result of aggression by neighbouring males, some suitable nest sites within a building may remain unused. Abandoned buildings, with numerous access points, and open barns or stalls may accommodate more pairs than small, well-kept buildings where it is more difficult for pairs to keep their distance and to find different points of entry (Snapp 1976). Nevertheless, large groups do form in suitable buildings with single access points (A.P. Møller, pers. comm.). The number of pairs nesting at a single site can vary widely from one to over 200 (von Vietinghoff-Riesch 1955; Cramp 1988; Møller 1994a; Brown & Brown 1999a). However, single pairs or groups of two or three are usual, while the majority of pairs nest in medium-sized to large groups (Cramp 1988). In Scotland, for example, group size was 1–14 pairs; half the sites had only one or two pairs, but sites with ten or more pairs held a fifth of the breeding population and the average number of pairs per site per year was 3.2–4.4 (Thompson 1992). In one four-year period in a site in Denmark (Møller 1983), there were 40 solitary pairs (14% of pairs), 27 groups of two (20% of pairs), six groups of three (7% of pairs), seven groups of four to six (12% of pairs) and nine groups of 7–22 (47% of pairs). In North America, pairs also typically breed alone or in small groups (Shields et al. 1988; Brown & Brown 1999a). Møller (1994a) did not find any latitudinal difference in the proportion of Barn Swallows breeding alone or in large groups. At natural nest sites, before Barn

14639.qxd

24/1/06

3:53 pm

Page 53

Social behaviour and vocalisations

53

Swallows nested on human artefacts, group size and structure were probably similar: cave sites usually also have only one or two nests or occasionally small groups of up to 30 (Speich et al. 1986). Group size varies between years, at least in large populations; in a year when the population increased, Thompson (1992) noted more groups with five or more pairs and fewer solitary pairs. Early in his long-term study, Møller (1983, 1991e) also recorded an increase in group size, and more small groups, with increasing population size. However, the Danish population has declined markedly since then: nest sites have been lost, but the proportions of Barn Swallows breeding in groups of different sizes at the remaining sites have not changed overall, except where the habitat has changed (Møller & Szép 2005a). In Europe, group size depends to a great extent on the type of habitat, livestock and especially dairy farms being preferred (Chapter 6). Vansteenwegen (1988), for example, recorded three pairs on average on farms with livestock compared to only 0.34 on farms without any livestock and 0.09 on houses. Ambrosini et al. (2002a) found that 40% of the variation in group size in their study could be explained by the presence of livestock and of traditional stabling, and Møller (1983) found that group size on farms increased with the area of animal stalls available. Groups are generally larger on farms with cattle than on other types of farm (e.g. Hölzinger 1969; Landmann & Landmann 1978). Loske (1994) recorded an average of 5.5 pairs per cowshed, 2.5 pairs per pig shed and only 1.0 pair in other buildings, and breeding groups were largest when cattle were present on farms. Møller (2001b) recorded groups averaging 9.53 on dairy farms, but these declined by 48% to an average of 5.00 after dairying had stopped on the farms. Similarly, Akopova et al. (2000) noted a decrease in the average number of pairs per farm from 12.6 to 4.7 between 1985 and 1997, attributed to a decline in livestock. More Barn Swallows can breed where there are plenty of good feeding sites: Loske (1994) found that the number of pairs was positively related to the amount of pasture, hedges, woodland and sources of water around the site, and Møller (1987d) recorded larger groups where insects were abundant and shelterbelts were present. There is also considerable variation in the population density, as suitable nesting sites may be clumped in otherwise unsuitable habitat. In areas with scant human habitation or few good feeding areas, such as upland moorland, there may be less than one pair/km2, whereas in areas where small farms and villages provide plenty of nesting and feeding sites there may be tens of pairs/km2 (Table 3.1; Chapter 6). Places with low-intensity livestock farming can have particularly high densities: in the Caucasus, an area with cattle had 105 pairs/km2, whereas a neighbouring one without cattle had only 27 pairs/km2 (Komarov 2000). Farmland in Western Europe with more intensive farming has much lower population densities (Table 3.1). Changes in habitat quality such as modernisation and intensification of farms are also associated with changes in population density, as seen in studies in the Czech Republic and Germany in the 1970s and 1980s (Table 3.1). Over larger areas, population densities vary widely, probably depending on the amount of suitable habitat available. In Europe, they vary from about 1,300–1,700 pairs/50×50-km square in

14639.qxd

24/1/06

3:53 pm

Page 54

54 Table 3.1.

The Barn Swallow Population densities of Barn Swallows in various habitats and localities.

Pairs/km2

Habitat

Locality

Source

0.7 1.7 3.7 3.7–11.8 4.4

Upland farmland Urban Urban Upland settlements Lowland mixed farmland

Scotland Japan Karelia, N Russia N Ossetia, S Russia Scotland

5–12 5.6 9.3 9.9 12.3–14.2 13.1 14–22 15.3 16.1 19.4 55.9 170.9–338.1

Farmland, late 1980s Farmland/villages, 1987 Arable Mixed farmland Farmland Farmland/villages, 1977 Farmland, late 1970s Mixed farmland Pasture/woods Riparian Villages Lowland settlements

Czech Republic Germany Germany Poland Estonia Germany Czech Republic Switzerland Germany Germany Karelia, N Russia N Ossetia, S Russia

McGinn 1979 Suzuki 1998 Artem’yev et al. 1993 Komarov 2000 Thompson 1992; Turner, unpubl. Kren 2000 Loske 1994 Loske 1994 Kartanas 2001 Kose 1994 Loske 1994 Kren 2000 Egger 2000 Loske 1994 Loske 1994 Artem’yev et al. 1993 Komarov 2000

Fennoscandia to 4,000–8,000 over much of Western Europe, where farming is predominantly intensive, and may be more than 10,000 in Eastern Europe, where farming is often low-intensity (Møller & Vansteenwegen 1997).

BREEDING IN GROUPS One frequently suggested benefit of group living is a feeding advantage, particularly when prey is patchily distributed in time and space, as is that of the Barn Swallow (Chapter 2). Members of the group may be attracted to areas where other individuals are foraging successfully, or they may follow successful foragers from the breeding site to good feeding sites (Ward & Zahavi 1973). Hebblethwaite & Shields (1990), however, did not find any evidence of Barn Swallows following successful foragers, at least during two seasons of generally good weather, although such information transfer may be more useful in very bad weather. Hoskyn (1988, cited in Brown & Brown 1999a) also found no evidence of Barn Swallows using the group as an information centre. Barn Swallows may benefit by joining already foraging swallows (Hebblethwaite & Shields 1990), but for most of the time they probably do not need the help of other individuals to find food. Unlike Cliff Swallows, which do follow colony

14639.qxd

24/1/06

3:53 pm

Page 55

Social behaviour and vocalisations

55

members to feeding sites (Brown & Brown 1996), Barn Swallows feed close to the nest and so, to some extent, probably know which are the best feeding sites in different weather conditions. Other studies have also not found a beneficial effect of group size on feeding success in Barn Swallows (Snapp 1973, 1976; Møller 1987d). The lack of synchrony in egg-laying and hatching also suggests that group activities such as foraging are unlikely to be important (e.g. Snapp 1973). Rather than increasing foraging efficiency, large groups may actually forage less efficiently by reducing the amount of food available and may require a large local insect population. Thus Møller (1987d) found that group size increased with increasing insect abundance (as measured by sweep net samples) and with the availability of sites where the Barn Swallows could feed in bad weather. The amount of food available for each pair was lower in larger groups, and group pairs had lower feeding rates than solitary pairs did, so there may be an upper limit to the number of pairs that can breed in an area. If there is a negative effect of group size on foraging it is likely to be small, however, or perhaps important only in seasons with persistent bad weather or where groups are very large. Møller (1987d), for example, did not find any difference in weight between broods of solitary and group pairs. Shields & Crook (1987) found the same result for chicks in nests without parasites; proportionally more chicks starved in large groups, but only slightly so. Snapp (1973, 1976), however, did find that chicks in large first broods in larger groups weighed less than those in small groups in one year of her study, and these broods had more runts and more variable weights within the brood, suggesting an effect of group size on chick growth when food was limited. Evans (2001) also found that chick condition (weight in relation to tarsus length) peaked at intermediate group sizes of about ten pairs, but whether poor condition in large groups was a consequence of reduced per capita food levels is not known. The other main potential advantage of being in a group is increased protection from predators. There are more eyes to spot a predator; a predator may be confused or deterred by large numbers of prey, especially if they mob it as a group; and with so many prey items available, any one individual is less likely to be the victim. Again, however, Barn Swallows do not seem to benefit much in this respect. They are more vigilant in large groups, detecting predators earlier, and mobbing is more intense, with more individuals taking part (Smith & Graves 1978; Møller 1984a, 1991h; Shields 1984b). However, predation on nests is low anyway (Chapter 9), so these benefits are likely to be small, and mobbing is done mainly by the pair whose nest is at risk, helped if at all by neighbours whose own nests may be threatened, so predator deterrence is not a group effort (e.g. Shields 1984b; Chapter 8). In addition, Barn Swallows take substantial risks, diving at predators and getting close to them, so do not benefit from the group mobbing seen in colonial hirundines such as Cliff Swallows, in which individuals mob together at a distance (Brown & Hoogland 1986). There are also disadvantages, as a large group may be more conspicuous and attractive to a predator, especially when large numbers of newly fledged young are present (Chapter 9). Indeed, predation seems either not to vary with group size or to affect large groups more severely (e.g. Snapp 1973, 1976; Shields & Crook 1987).

14639.qxd

24/1/06

56

3:53 pm

Page 56

The Barn Swallow

A major disadvantage of being in a group is the abundance of parasites. Barn Swallows, both adults and chicks, are hosts to many parasites, which can reduce fledging success and survival (Chapter 9), and these are more of a problem in larger groups. Nests are more likely to be infested with mites or blow fly larvae as group size increases and numbers of blow fly larvae also increase (Møller 1987d; Shields & Crook 1987). Large groups may suffer more from parasites partly because nests are close together, social contact more frequent and transmission of parasites more likely, and partly because of other characteristics of the group: in New York State, pairs in large groups started breeding late in the season when parasite infestation was higher anyway (Shields & Crook 1987). Some other causes of mortality, such as egg losses (some of which are due to both male and female conspecifics tossing out eggs), infanticide and nest falls can also be greater in large groups (Shields & Crook 1987; Hoskyn 1988, cited in Brown & Brown 1999a; Møller 1988b, 1994a; Chapter 5). Studies of breeding success have not found that large groups are better. Some have reported no relation between group size and fledging success (e.g. Snapp 1973, 1976; Ambrosini et al. 2002a; Safran 2004) or more fledglings for small or mediumsized groups (Lohoefener 1977, 1980; Shields & Crook 1987; Loske 1994). At least in part, variation in breeding success between groups of different size can be explained by differences in age or other characteristics of the groups’ members. Large groups in Shields & Crook’s study, for example, included more first-years than small groups did. Studies that have taken such factors into account have found that breeding success does not vary with group size (Safran 2004) or peaks in intermediate groups (A.P. Møller, pers. comm.). There are some social benefits to living in a group, such as more opportunity for copulating with partners other than the social mate, getting a mate by infanticide or dumping eggs in other pairs’ nests (Chapter 5). But these benefits entail costs as well, such as having to guard the nest and mate more (Møller 1987d, 2004a). The costs and benefits sometimes vary with the number of pairs at a site. Møller (1991e) reported that relatively more females mated with males outside their pair bond in large groups, and males had to do more mate-guarding to prevent it. However, Safran (2005) found no relation between group size and a male’s paternity in his social mate’s brood in a North American population. Some individuals may sometimes benefit from being in a breeding group. A long-tailed male, the sort preferred by females, may thus have increased opportunities to mate with other females, whereas a short-tailed male risks being cuckolded. However, large groups are not necessarily best for long-tailed males. Møller (2002a) found no overall relation between male tail length and group size: long-tailed males were associated mainly with large groups in some years and with small ones in others. The relative benefit of a large group may also vary with the bird’s age: a young bird may gain from the extra vigilance, but a more experienced one may not (Brown & Brown 1999c). In New York State older pairs were often solitary or in small to medium groups (Shields & Crook 1987). In addition, there is a genetic component, with offspring nesting, at least in their first breeding season, in similar group sizes, and at similar distances to their neighbours, to those of their parents (Møller 2002a). Even when Møller moved chicks to

14639.qxd

24/1/06

3:53 pm

Page 57

Social behaviour and vocalisations

57

nests in other groups, so that they were reared by strangers, they still chose a social environment like that of their biological parents. Thus some individuals may be suited to living in small groups and others in large ones. However, once a Barn Swallow has chosen a site it is generally faithful to it, even if the group size changes in later years (Chapter 10). Another reason why some species of bird nest in groups is that nest sites may be limited, forcing pairs to nest together, while the type of site that is suitable for attaching a nest, such as a cliff face, bridge or barn, may often have enough space for more than one, allowing groups to develop. Snapp (1973, 1976) suggested that this was true for Barn Swallows in North America as she did not find any benefits of living in a group related to foraging, predation or the number of fledglings reared, whereas buildings that were large or had more access did house larger groups. Brown & Brown (1996) also suggested that they do not benefit from nesting close together and that breeding populations are limited by the availability of nest sites, as they found that Barn Swallows do not clump their nests together (see above). Nest site limitation is unlikely to be the whole explanation for the formation of groups in Barn Swallows, however, because more pairs can fit themselves on to a site when population density is high (Møller 1983, 1987d). In addition, sites large enough for a group may have a single pair, some sites have single pairs one year and groups of various sizes in others, and some are unused in some years and used in others (e.g. Holroyd 1975; Lohoefener 1977, 1980; Møller 1983; Shields et al. 1988), suggesting that factors other than availability of nest sites determine which are used. The presence of livestock, for example, is more important in determining group size than is the availability of nest sites, with group size declining on farms when cattle are sold (Møller 2001b; Ambrosini et al. 2002a,b). Other hypotheses to explain why birds breed in groups consider the quality of the site itself. In a variation on the idea of nest site limitation, Shields et al. (1988) suggested that individuals are attracted to traditional good-quality sites, where there is evidence of other Barn Swallows breeding. The fact that other pairs have nested successfully there suggests that a newcomer will be able to breed there too. In contrast, an otherwise suitable site that does not have Barn Swallows already breeding may have problems that are not immediately apparent. For example, it may be regularly flooded or exposed to predators later in the season, leading to failure of any breeding attempts. Thus groups of three or more are likely to persist between years, whereas sites with single nests may not persist (Møller 1983). Another idea is that, if sites maintain their quality over time, birds may settle at sites in relation to the resources available there or, alternatively, that a fraction of the population chooses a site because of its resources, while other birds are then attracted to the site by their presence (Brown & Rannala 1995). Barn Swallows may learn about good breeding sites both as juveniles and as adults and they could use a variety of cues to do so. They could assess the breeding success of other individuals at a site from, for example, the number and size of broods being fed (e.g. Danchin et al. 1998). After reaching independence, juvenile Barn Swallows are known to wander and visit other breeding groups, possibly checking out where

14639.qxd

24/1/06

58

3:53 pm

Page 58

The Barn Swallow

other Barn Swallows are breeding successfully (Chapter 10). Since first-years breed later than older Barn Swallows, they could also do this in the following spring. Late arrivals, probably first-years, in Scotland generally joined sites where three or more pairs were already breeding (Thompson 1992). Alternatively, first-years could look for evidence of previous breeding at a site, such as old nests (Shields et al. 1988). In this case the evidence for breeding is also a resource, as Barn Swallows benefit from breeding in old nests rather than building new ones (Chapter 6; Safran 2004). It is unlikely, however, that Barn Swallows use mainly the breeding success of others to decide where to breed themselves, because this can be an unreliable cue (Safran 2004). Pairs at different sites within a general area can have similar success in any one year, whereas unpredictable weather can result in success varying from one year to the next. So there may be little to choose between sites and no guarantee that a chosen site will remain good. In addition, Safran (2004) found that groups do not grow in size in proportion to how successful breeding was the previous year, suggesting that Barn Swallows are not attracted by this cue. In contrast, Safran did find evidence that Barn Swallows use the presence of old nests to decide where to breed. When she removed nests from sites during the winter, relatively fewer immigrant females subsequently settled there than at control sites where nests were left, and than in the year before the nests were removed. In addition, the number of breeding pairs and the number of immigrant females at a site depended to a large extent on the number of old nests present at the start of the season (Figure 3.1), and group size declined when Safran removed nests over winter. Immigrants thus seem to be attracted to settle at sites with old nests. They also seem to make their decision at the start of the breeding season, although a preliminary knowledge of local sites may be gained the previous summer and the final decision made in spring. The traditional site hypothesis is supported by Ambrosini et al. (2002a, b) in their study of 121 farms in Italy. They found that the distribution of Barn Swallows was related to the presence of livestock on farms in previous years and was best predicted by the presence of livestock seven to eight years before they censused the Barn Swallows, rather than during the census itself. Farms with livestock constitute highquality breeding sites, but the number of such farms had been declining during the study period. There thus seems to be a lag in the response of Barn Swallows to changes in site quality. In part this is because Barn Swallows are faithful to their breeding sites, returning to the same site each year (Chapter 10), but this cannot be the sole explanation, as most live only a couple of years. However, if initially goodquality sites become traditional sites, young birds would continue to be attracted by the presence of nests or Barn Swallows already breeding there, even if the quality of the site declines. In addition, high-quality nest sites may remain on the farm when the livestock have gone (Ambrosini et al. 2002a,b). However, Møller (2001b) found that more first-years recruited to farms when these had dairy cattle than when they had ceased dairying, suggesting that young Barn Swallows are attracted to highquality sites, perhaps by the already large group breeding there. The more severe weather in spring in Denmark, and other high-latitude sites, than in Italy may make

14639.qxd

24/1/06

3:53 pm

Page 59

Social behaviour and vocalisations

59

Figure 3.1. (a) The number of breeding pairs of Barn Swallows and (b) the number of immigrants settling at a site increase with increasing numbers of old nests at the site at the start of the breeding season (expressed as natural logarithms, ln). Reprinted from Safran 2004.

the quality of the habitat more important for young Barn Swallows there than the mere presence of nest sites (Ambrosini et al. 2002b).

SONG Barn Swallows have a number of songs and calls, used in a variety of contexts (Bergmann & Helb 1982; Cramp 1988; Brown & Brown 1999a). Vocal communication is important between members of a pair and of a family, and between potential mates and competitors. European males sing a pleasant rapid twittering song which often ends in a harsh rattle. Sometimes a terminal whistle ‘su-seer’, with the second part falling in pitch,

14639.qxd

24/1/06

60

3:53 pm

Page 60

The Barn Swallow

follows the rattle, but this is not very frequent; in one study the whistle was produced regularly by only 18 of 48 individuals (P. Galeotti, unpubl. data). Incomplete songs, without the rattle, are often sung first thing in the morning (L.Z. Garamszegi, pers. comm.). Males sing while in flight or when perched, and occasionally from the ground, but usually at the nest site. Females do not sing the full song of the male but often twitter. Young males, at about a month or more old, possibly soon after fledging, sing a subsong, which is a series of short, quiet phrases. This develops into the full song. It is not known when and from whom males learn the song; they might learn from their father, neighbouring males or even males from other groups, which they often visit before migrating (Galeotti et al. 2001; Chapter 10). The song continues to develop during the males’ first year (see below). Males sing mainly in the breeding season but also sometimes in the winter quarters before returning in the spring (von Vietinghoff-Riesch 1955). Males sing two types of song: type A and type B (Galeotti et al. 1997; Figure 3.2). Type B song is more stereotyped than type A, and consists of simpler vocalisations and contact calls. Both type B and the more complex type A, however, usually end with a rattle, and both are sung by males at the nest site. A bout of singing includes both types, sometimes with and sometimes without the rattle, averages three songs (range 1–17) and lasts for about 11 seconds (range 2–51 seconds). Between bouts of singing a male may be silent or make chittering calls, sometimes for a second or so, sometimes for many minutes. A type A song lasts for about four seconds on average (range 1.7–7.8 seconds), with a half-second rattle and is composed of about 20 syllables (average 19.8, range 9–34 in Italy: Galeotti et al. 1997; Saino et al. 2003f ), of different types, which vary in fundamental frequency from 840 to 1,500 Hz and in peak frequency from 7,300 to 9,200 Hz (Figures 3.2, 3.3). The rattle is a high-frequency (5,560–6,600 Hz) syllable consisting of a number of pulses of sound. Songs are varied, each including several types of syllables, each of which may be repeated several times and sung in different sequences. Each male has many (17–36 in Italy and 16–30 in Spain) different syllable types in his repertoire, using most of these in each song but usually not repeating a particular sequence in different songs (Galeotti et al. 1997; P. Galeotti, unpubl. data; L.S. Garamszegi, pers. comm.). A male’s repertoire size can be estimated from as few as five songs (L.S. Garamszegi, pers. comm.). Song content also varies between groups, sometimes to a large extent even when the groups are near each other (Saino et al. 2003f; N. Saino, pers. comm.). In a study in Italy, the syllable repertoire increased logarithmically with the number of Barn Swallows in the group, reaching an asymptote at groups of six (P. Galeotti, unpubl. data). Males vary in many characteristics of the type A songs they sing, particularly in the rattle, which may indicate to other Barn Swallows something about the quality of the singer. Galeotti et al. (1997) found that large males sing low-frequency rattles. The frequency of the song is inversely related to its length and to the number and type of syllables, so males with long complex songs also have low-frequency ones (Saino et al. 2003f ).

14639.qxd

24/1/06

3:53 pm

Page 61

Social behaviour and vocalisations

61

Figure 3.2. Sonagram of (a) type A and (b) type B song of a male Barn Swallow, recorded in Italy. The song is composed of a number of different syllables. The recording was analysed with the Avisoft Sonagraph package, the bandwidth was 200 Hz and the frequency resolution 80 Hz. Reprinted from Galeotti et al. 1997, with permission from Elsevier.

Singing is affected by the male hormone testosterone in many bird species, but it also varies with ecological and social circumstances. Male Barn Swallows with high levels of testosterone in the blood sing long rattles with a large number of pulses,

14639.qxd

24/1/06

62

3:53 pm

Page 62

The Barn Swallow

Figure 3.3. Repertoire of syllables in the songs of an Italian Barn Swallow population. Syllable R is the rattle. Reprinted from Galeotti et al. 1997, with permission from Elsevier.

perhaps indicating their level of aggressiveness (Galeotti et al. 1997). However, the rates of singing and the number of syllable types in the song do not correlate with testosterone levels, perhaps because of other, social, factors (Saino & Møller 1995a; Galeotti et al. 1997).

14639.qxd

24/1/06

3:53 pm

Page 63

Social behaviour and vocalisations

63

Males also vary their songs depending on who is listening. They sing more frequently when they are in large groups (Møller 1991f ). In Galeotti et al.’s study, the rate of singing did not vary with the immediate number of neighbours, at about the same stage of breeding, that a male had. However, the number of neighbours did affect the songs’ quality: the more there were, the more type A songs the males sang, and these were short with few syllables and included long, high-frequency rattles. Males also sang similar songs to those of their nearest neighbours. Songs are short and repetitive mid-season when social competition is high (Galeotti et al. 2001). When they have few competitors, for example in small groups or early or late in the season, males sing more varied and longer songs (Galeotti et al. 1997, 2001). Males may sing short songs to avoid having them overlapped by those of other males. In song contests between two males, matching and overlapping songs may be a way of sizing each other up, and an overlapped song may indicate that the singer is not as good a male as the one overlapping his song; potentially, females could use this information when choosing a mate (Galeotti et al. 1997; Gil & Gahr 2002). Studies in Italy (Galeotti et al. 2001; P. Galeotti & N. Saino, unpubl. data) show that some features of the song vary with the age of the male. Males older than a year sing longer songs, with more types of syllables, and repeat sequences of syllables more than first-years do. As well as comparing males of different ages within a season, Galeotti et al. also followed individual males between years and found that they increased the length of their song and changed the syllables they sang. In contrast, a male’s rattle is consistent over time. The rate of singing is also independent of the male’s age. A recent study in Spain found that songs of older males, as well as being longer, also had a lower peak amplitude frequency than those of first-years (Garamszegi et al. 2005). As well as being a good guide to a male’s age, the song provides further information about the singer’s health. In a Spanish study, males with few or no lice sang longer songs than those with heavy infestations, and males with a healthy immune system sang songs with a low peak frequency rattle (Garamszegi et al. 2005). Singing rate may also guide females to choose the healthiest males (Chapter 4). Parasites, and pathogens in general, may weaken males, affecting their ability to sing, and also require the birds to spend more time feeding, and hence less time singing. Males sing less frequently when their nests are infested with mites: Møller (1991f ) found that males sang less during their mate’s next fertile period when he added mites to the first-clutch nest than did males whose nests were left alone or those whose nests were sprayed to remove mites. Singing was reduced even more when the first clutch was enlarged by one egg; Møller suggested that this was because males had to work harder so were in poorer condition. Males that sing at high rates also have low blood lymphocyte and antibody levels, which may indicate that they are relatively free of pathogens (Saino et al. 1997a). However, song is only weakly related to tail length so does not indicate the overall quality of males (e.g. Møller 1994a; Saino & Møller 1995a; Møller et al. 1998a; Chapter 4). Saino et al. (2003a) examined the effect of experimentally increasing and reducing tail length on song quality. They found that males with artificially

14639.qxd

24/1/06

3:53 pm

Page 64

64

The Barn Swallow

lengthened outer tail feathers sang songs with longer rattles and more pulses than males with shortened tails, perhaps because of more interactions with other males, which might have perceived them as more serious competitors, or with females seeking extra-pair copulations. However, song length and complexity did not vary with tail length. Like other songbirds, male Barn Swallows probably direct their singing both to females – to attract potential mates and, once mated, to stimulate breeding behaviour and egg development – and to males, to keep competitors away (Møller 1990e, 1991f ). Different aspects of the song may have different functions in this respect. A varied repertoire may impress females, while the rattle, which is most prominent at the time pairs are forming, may be a signal of aggression. However, females may also want to mate with aggressive males, so might also be attracted to those singing short songs with long rattles when other males are present (Galeotti et al. 1997). Males probably sing for different reasons at different times. They sing over a long period, from the time of their arrival until their mates are incubating, but particularly at the time the females are laying eggs (Møller 1994a; Saino et al. 1997a). Songs at the latter stage may deter other males that are seeking copulations with already mated females and may maintain the males’ attractiveness to their mates. Males, especially long-tailed ones, that sing at a high rate father more of their mates’ broods, that is, their females seek fewer copulations with other males (Møller et al. 1998a). During incubation, on the other hand, males may sing to attract other copulation partners of their own (Saino et al. 1997a; Chapter 5).

OTHER VOCALISATIONS As their name implies, contact calls are used to maintain contact between individuals in pairs, families or flocks and can be used throughout the year, at the nest, and among feeding or migrating groups. They are also given when the birds are alarmed. The principal call is a ‘witt-witt’, given singly or repeated. However, contact calls are often run together into a monotonous twitter, rather like the song but without the rattle, and produced by both males and females. This twitter call is given by pair members while in flight or at the nest, and is used as a greeting. Males will twitter at the nest after feeding the chicks and often twitter before producing the full song. Females have their own contact call, a ‘tir-huit’ with which they call their mate to follow them during nest-building and entice fledglings away from the nest. Parents feeding chicks give a high-pitched call as they arrive at the nest to induce the chicks to beg (e.g. Sacchi et al. 2002). A number of calls are associated with attracting mates and maintaining the pair bond. Unpaired males give a call sounding like ‘it-it-it’ when courting females and utter a series of ‘wi-wi-wi’ notes, likened to a rusty hinge on a gate by Purchon (1948), to attract females to a nest site. The same call is used to entice fledglings to a roost site. When copulating, males call ‘wieh-wieh’.

14639.qxd

24/1/06

3:53 pm

Page 65

Social behaviour and vocalisations

65

Alarm calls are directed at both conspecifics during disputes and predators. Both sexes utter a screeching sound in confrontations. Both, especially females when incubating, also use a ‘chirr-chirr’ call apparently to drive off the partner’s unwelcome attentions. The same call is uttered when a predator is seen some distance away. The main alarm call, however, is the familiar ‘tsi-wit’, with a higher-pitched second than first syllable. This is frequently heard when predators are nearby or when males find intruders on their territories. Other alarm and distress calls include a ‘dschiddschid’ given in flight, a lowpitched ‘flüh-flüh’ when chased by a Peregrine, a soft ‘dewihlik’, and a sharp ‘weerweer’ when caught by a predator (or human). There is also a low-pitched, slurred two-note call, which has usually been recorded when a Eurasian Hobby is present, but also with a Eurasian Sparrowhawk and a stooping Peregrine, and may be an urgent warning call in particularly dangerous situations (Atherton 1998 and see editorial comment and subsequent letters in British Birds 92: 51–52, and 95: 193). A few other calls and sounds have been recorded: an incubating female making a cackling sound on leaving the nest, and incubating and roosting birds snapping their bills. This latter sound is also made during courtship. North American Barn Swallows have a similar variety of songs and calls to the European ones (see Samuel 1971a; Brown 1985; Brown & Brown 1999a). They have a similar twittering song, lasting 4–20 seconds or more and ending in a ‘rattle’ of 9–12 notes; a chirping contact call, given singly or repeatedly, often before, after or during the song; stuttering threat or anger calls directed at conspecifics, during chases and fights; and mild and intense alarm calls given singly or repeated (the ‘cheep’ call used in any alarm situation and the ‘churee’ whistle used when a predator is close by). Samuel (1971a) recorded females giving low-intensity stutters when chased by males, and both sexes use high-intensity stutters as threats to conspecifics. Both sexes have a repeated whistling call, similar to the courtship call of rustica, used to maintain the pair bond; males relieving females during incubation have also been known to give this call. Females give a whining sound, repeated two to six times and often accompanied by twittering, before copulation and a rapid whine during nest site selection. Brown (1985) also recorded a repeated ‘cheet’ call which parents used before, during and after feeding fledglings; this call may help the fledglings recognise their parents (see below). Chicks start to make a begging call when about three days old. At first the call is weak and barely audible but, as the chicks develop, the call becomes stronger and more persistent, changing from a ‘si-si’ to a ‘twiet-twiet’ near fledging, by which time it sounds like their parents’ contact call. As the chicks grow, the syllables in the call lengthen and the intervals between syllables shorten (Saino et al. 2003a). As the parent approaches with food, the ‘twiet-twiet’ changes to a ‘dsched-dsched’. North American Barn Swallow chicks and fledglings have a similar juvenile call. Once fledged, the young Barn Swallows have two main calls. The ‘wee-wee’ is a begging call, used to solicit food from adults, while the ‘üit-üit’ call is given when a predator is seen. The predator call becomes identical to the adult’s alarm call by the age of 30–40 days.

14639.qxd

24/1/06

66

3:53 pm

Page 66

The Barn Swallow

PARENT–OFFSPRING RECOGNITION Despite the possibility of other females dumping eggs in their nest (Chapter 5), Barn Swallows do not recognise their own eggs. They readily accept and incubate eggs from other nests put into their own during the egg-laying and incubation stages, although they will eject eggs appearing before they have started laying their own clutch (Burtt 1977; Grzybowski 1979; Møller 1987c). Barn Swallows also usually remove any eggs that appear damaged (Mallory et al. 2000). Numerous experiments have shown that Barn Swallows will feed alien chicks placed in their nest just as much as their own offspring and will feed fledglings that have landed there (Chapter 8). Parents appear to be aware of, and will sometimes peck at, intruders when these are of a different age from their own young but they will still feed them (Grzybowski 1979; Ball 1982). Even fledglings of different species are not necessarily discriminated: Barn Swallows have been recorded feeding a fledgling Tree Swallow, even though their own chicks were only 14 days old (Butler & Campbell 1987). Colonial species of hirundines start to tell their own from alien young at about the time they fledge, when the chicks’ calls (and plumage signals, such as the facial pattern in Cliff Swallows) become individually identifiable, but Barn Swallows fail to do this (Beecher et al. 1986), even ignoring obvious plumage differences in the case of the Tree Swallow. North American Barn Swallow young, whether from the same or different families, have similar calls, which typically start with a burst of noise and have two frequency bands. The calls lack any repetitive frequency modulation, which the more elaborate calls of young Cliff Swallows, in contrast, do contain. Consequently it is difficult to identify individual Barn Swallows by their calls, or to determine whether they are related, whereas individual Cliff Swallows’ calls are distinctive and the calls of two siblings are more similar than are the calls of two unrelated chicks (Medvin et al. 1992, 1993). Loesche et al. (1991) investigated how easily adult Barn Swallows, Cliff Swallows and European Starlings could tell apart tape-recorded calls of different swallow chicks, either Barn or Cliff. The scientists trained the birds by giving them food when they pecked at a particular spot in the experimental apparatus to indicate that the two calls played to them were different. The birds found it much easier to discriminate between two Cliff Swallow calls than between two Barn Swallow calls. That Barn Swallows do not distinguish their own from alien young is thus probably at least partly because there are only poor cues to identify them, rather than that they can recognise differences but ignore them, although this may be a factor because there seems to be little need for discrimination to evolve. Because Barn Swallows do not nest very close to each other and because they sequester their fledglings in a tree or barn away from other family groups, the adults have little need to distinguish their own young from those of other parents. They may recognise their family primarily by its location in their own nest or at a specific site outside. Fledglings therefore have few distinguishing features. This is in contrast to colonial species of hirundines, such as Cliff Swallows, whose newly

14639.qxd

24/1/06

3:53 pm

Page 67

Social behaviour and vocalisations

67

fledged young may land in neighbouring nests and where fledglings frequent crèches, often containing tens or even hundreds of individuals. Barn Swallow chicks, however, can recognise their parents’ calls, although apparently not as well as Cliff Swallows recognise theirs, as they respond less often to recordings of them in experiments (Medvin & Beecher 1986). Fledglings outside the nest will call to their own parents approaching them with food but not to other Barn Swallows (Medvin & Beecher 1986). Why do fledglings recognise parents and not vice versa? The fledglings that recognise and respond to a parent may be the first to get fed, without wasting energy begging from every Barn Swallow that passes by (Medvin & Beecher 1986). Although broodmates have similar calls, males and females do develop slightly different ones. At 12 days of age it is not possible to distinguish between males and females when they are begging but, by 16 days, Saino et al. (2003a) could classify 86% of chicks as either male or female, based on a combination of the length of syllables, the length of the interval between syllables and the frequency of the peak amplitude. The differences in calls may be the result of early sexual differentiation of the vocal system, as males will go on to develop a more complex song (Saino et al. 2003a). Whether the parents recognise the sex of their offspring by their calls and favour one or other sex is not known. Apart from the calls, male and female chicks are indistinguishable.

14639.qxd

24/1/06

3:53 pm

Page 68

CHAPTER 4

Attracting and choosing a mate From all my observations, it constantly appeared that each sex has the long feathers in its tail that give it that forked shape; with this difference, that they are longer in the tail of the male than in that of the female. Gilbert White, 1789

Barn Swallows in Western Europe have been the subject of many years of research, especially on what females look for when choosing mates and the costs and benefits of these characteristics. North American and other races have received much less attention, and so our knowledge of mate choice in Barn Swallows is very biased. This difference is being rectified, with studies in North America now underway, but what follows refers mainly to European Barn Swallows.

14639.qxd

24/1/06

3:53 pm

Page 69

Attracting and choosing a mate

69

MATING BEHAVIOUR Males sing and display to females on the wintering grounds and on migration and some pairs may form then (Cramp 1988), but males and females usually arrive at the breeding grounds separately. The first to arrive are the older males who lay claim to a breeding site of a few square metres with a nest or potential nest site. The males sing and chase off other males from their chosen site. The nesting territories at a breeding site may not vary much in quality; Møller (1994f ) found that they were not occupied in a consistent order each year. In addition, pairs usually return to a site they used the previous year or to another nest close by (Chapter 10). If both members of a pair survive they may therefore meet up at their old nest site (Shields 1984a). When they arrive, unpaired males try to attract partners by singing and showing off their tails. The tails are spread wide during this display to reveal the white spots. Males, both those with and without mates, often display communally, gliding or flapping slowly high above the nesting sites and singing, for an hour or more. Once a male has a female’s attention, he flies to his nest site, or potential nest site, but he may have to fly back to her and then to the nest site several times if she does not follow him immediately. When she does go to the nest site, the male lands, still fanning his tail, and utters enticement calls. When she lands, he sings and then lowers his head and pecks towards the nest site. If the female is not impressed, he may need to show her another site, or try to attract another female. If the female leaves, she may do so immediately or after several days (range 1–16 days), but a female generally finds a partner within three days of arriving (Møller 1985, 1994a). A male, in contrast, may court two or three females before mating, if he mates at all, and can take from only one day to as long as 31 days to get a mate (on average 4.8 days; Møller 1994a). Barn Swallows will use outside roofs, trees and overhead wires, as well as the nest site, to copulate. A male solicits copulation by singing when the female is nearby. He then hovers over the female and fans his tail. If accepted, he mounts and copulates, uttering a copulation call. An acquiescent female may hold her body horizontally, with wings slightly open and lowered. The copulation is over in a few seconds and may be followed by preening. A female sometimes rejects the male, turning round, raising the wings in a threat, pecking or flying off. Copulations are most frequent early in the morning (Møller 1987f ). Female birds are generally fertile for only a short period, usually from five days before laying the first egg until the day before the last one is laid. They can store sperm in their reproductive tract for several days: on average sperm can fertilise an egg up to five days after copulation (Birkhead & Møller 1992). Barn Swallows will copulate over a longer period than this, however, starting after pairing (Møller 1994a). When the interval between pairing and egg-laying is lengthy, copulations can occur at a high rate for two to three weeks. Pairs copulate less during the egglaying period and stop in the first few days of incubation. During the females’ fertile

14639.qxd

24/1/06

3:53 pm

Page 70

70

The Barn Swallow

period, pairs copulate on average 1.5 times an hour for the first clutch (range 0–20) and 0.8 times for the second (range 0–13) and they may copulate over 50 times per clutch (Møller 1994a).

FEMALE MATE CHOICE A number of related features of the male’s plumage and song are involved in mate choice. Many studies have looked especially at the role of the male’s tail which has longer, elongated outer feathers relative to the female’s tail, and is markedly more variable. More recently, researchers have started to assess the importance of song and of plumage colour, such as the white tail spots and red throat and forehead (and the rest of the underparts in North American Barn Swallows). In Europe, at least, males with long tails are clearly the choice of discerning females; these males are more likely to get both mates and extra-pair partners than are short-tailed males and they also mate more quickly and court fewer females before being accepted (e.g. Banbura ´ 1986; Møller 1994a; Møller & de Lope 1994; Møller & Tegelström 1997; Saino et al. 1997e). In an elegant experiment, Møller (1988a) showed that females prefer long-tailed males. He shortened the tails of some males by cutting out a 20 mm-long piece from the base of each outer tail feather and gluing the rest of the feather back together; these males then had an average tail length of 85 mm. He lengthened the outer tail feathers of other males by gluing a 20 mm-long piece of feather to the middle of the feather; the tails were then 127 mm long on average. The new tail lengths were in the natural range of 85–146 mm. He also used two control groups to test for any effect of handling the birds and cutting the tail feathers. In one control group he just cut the tail and glued it back together without changing the length and in the other he left the tail as it was. Males were randomly allocated to the groups so there was no confounding effect of age. Møller found that the males with elongated tails got a mate within only a few days, whereas those with shortened tails took more than four times as long, frequently being rejected by females even though they displayed and sang just as much; the males’ success in the control groups was intermediate (Figure 4.1). In a similar experiment in Ontario, Smith & Montgomerie (1991) found that partners of males with elongated tails laid earlier, but few birds were studied and the researchers did not know whether the males were unmated at the start of the experiment, so it is not clear whether the females chose mates with long tails or laid earlier once mated to preferred males (Møller 1994a). In another, correlative, study in Ontario, males with long tails bred earlier and sired more offspring, including extra-pair ones, than short-tailed males, although differences in age might have been a factor (Kleven et al., in press b). Other studies in North America, however, have not shown a consistent correlation between male tail length and the timing of laying of their mates and other measures of seasonal reproductive success (Briceno 2002; Safran & McGraw 2004).

14639.qxd

24/1/06

3:53 pm

Page 71

Attracting and choosing a mate

71

Figure 4.1. Female Barn Swallows prefer males with long tails. Males with artificially lengthened tails paired sooner than those with unaltered or shortened tails. (Controls: feathers cut and re-glued or left unaltered.) Vertical lines represent standard deviations. Reprinted from Møller 1988a with permission.

Perfect mates need other qualities besides long tails. Females also like males with symmetrical tails, that is, with outer tail feathers of the same length. Males that get mates have more symmetrical tails than those that do not (Møller 1994c) and males with symmetrical tails also acquire mates more quickly (Møller 1994a). Møller showed this by changing the asymmetry of males’ tails, in one experiment by cutting or fixing pieces on the tail, in another by applying white correction fluid to mask the tips of the tail feathers (Møller 1992d, 1993d). The more symmetrical males mated earlier. Both tail length and asymmetry were manipulated in Møller’s (1992d) experiments and both affected how quickly the males acquired mates. These experiments have been criticised, as in the first the males’ flying ability might have been impaired, while in the second the tail might have looked abnormal (e.g. Evans et al. 1994; Møller 1994d; Swaddle & Cuthill 1994). Tail symmetry is closely associated with tail length (Møller 1994c), and its contribution as an additional indicator of good males may be relatively low when the level of asymmetry is small. However, in a 16-year study in Denmark, Møller (pers. comm.) still found a strong effect of asymmetry on mating success, independent of tail length. Large tail spots are also a sign of good mates. In experiments in which they reduced the size of the spots of some males with black ink, Kose & Møller (1999) and Kose et al. (1999) found that these males’ partners were less likely to have a second brood and so had fewer fledglings over the whole season. Reducing the spot

14639.qxd

24/1/06

72

3:53 pm

Page 72

The Barn Swallow

size thus seemed to make the males less attractive as mates. Kose & Møller (1999) suggested that the white spots would be a particularly useful signal to females at or around the nest site, originally in caves and now often in buildings, where it may be too dark for the tail length and symmetry to be apparent. In addition, males with bright red coloration, which are also generally long-tailed males, are better at attracting mates than paler males (e.g. P. Ninni et al. unpubl. data, cited in Perrier et al. 2002). In contrast, unlike in some other bird species such as Blue Tits, the ultraviolet component of the feathers does not influence the females’ choice of mates in Barn Swallows (Perrier et al. 2002). In a North American study, males with brighter coloration had partners who laid eggs earlier, suggesting that they were preferred as mates, and, unlike European Barn Swallows, the coloration of the males was not related to their tail length or to tail symmetry (Safran & McGraw 2004). However, experimental evidence for North American females’ preferences is lacking. Finally in this list of attributes of good-quality mates, European females also find males that sing at a high rate attractive (Møller et al. 1998a; Chapter 3). Being choosy about mates has its disadvantages. Females must spend precious time searching for the right ones, sometimes visiting several over a number of days (up to a week, Møller 1994a) before choosing. Once they have chosen a mate they may still change their minds and switch to another one (Møller 1985). The resulting delay in mating can affect breeding success, which declines over the season (Chapter 7). Females that try to mate relatively late in the season also have fewer and lowerquality males from which to choose, because the best ones will already have found partners. Those that do mate with the higher-quality males pay a cost later, however, because these females contribute relatively more to rearing the brood (see below). Females need to choose mates that provide them with either indirect benefits such as offspring that are also long-tailed and therefore sexually attractive, or that are healthy and long-lived, or direct benefits such as help with feeding the chicks. A long tail may not necessarily be a useful characteristic for breeding partners to have but it may be linked to other desirable inherited traits that will be passed on to the females’ offspring. Females choosing males by their tail length may thus indirectly be choosing males with ‘good genes’, such as genes that confer viability and resistance to infections (Hamilton & Zuk 1982; Møller 1994a). How can females be certain that a male with a long tail has good genes? Characteristics such as tail length may be signals that reliably indicate the males’ quality because they impose a cost that goodquality birds can bear better than low-quality ones can (Zahavi 1975; Grafen 1990; Iwasa et al. 1991; Møller 1994a; Kose & Møller 1999). Tail length itself is in part passed down from father to offspring: long-tailed males tend to have long-tailed sons, so females paired with them will have long-tailed sexually attractive sons (Møller 1991d, 1994a). This seems to be a genetic effect rather than, for example, fathers and sons being reared in similar environments or sons of long-tailed fathers getting better parental care and so being larger overall (Møller 1994a,g). Tail manipulation experiments thus show no effect of a male’s experimental tail length on size or tail length of his offspring or overall parental care (Møller 1994a), and males’ tails are of similar length to those of their biological sons, but not

14639.qxd

24/1/06

3:53 pm

Page 73

Attracting and choosing a mate

73

to those of males that were reared in their nest but sired by another male (Saino et al. 2003g). Tail symmetry is also in part inherited (Møller 1994c), so females mated to males with symmetrical tails tend to have sons with symmetrical tails. Long tails indicate that the owners are healthy. Males vary in their resistance to parasites and in their immune response (Saino et al. 1997b) and thus in their ability to grow showy feathers. Sickly males do not have the resources needed for extravagant feather growth. Male Barn Swallows with naturally long tails are better able to cope with diseases and parasites, as their immune systems respond more strongly to antigens than those of short-tailed males (Saino et al. 1995, 2002d, 2003d; Saino & Møller 1996). They also have low blood levels of the stress hormone corticosterone and so may be less susceptible to stress than short-tailed males (Saino et al. 2002d). An ability to resist parasites is a heritable trait, at least in part (Møller 1990b; Saino et al. 1997b), so long-tailed males in Europe pass this characteristic on to their offspring (Møller et al. 2004a). However, in a study in Ontario, there was no evidence of inheritance of the immune response, and the tail length of the biological fathers had no effect on their offspring’s immunity (Kleven et al., in press a). Parasites are a particularly important aspect of males’ health, although their effect may vary between localities and between years. Some males are more resistant to parasites, having a less serious infestation of mites and feather lice for example, than others (Møller 1991b; Møller et al. 2004a). Males with few mites and lice are more likely to acquire a mate and do so more quickly, and males with long tails have fewer of such parasites than those with short tails (Møller 1991b, 1994a; Saino & Møller 1994; Saino et al. 1995; Kose & Møller 1999). The presence or absence of parasites may thus reflect the quality or current condition of males. A male that is resistant to mites and lice has offspring that also have fewer parasites (Møller 1990b; Møller et al. 2004a; Figure 4.2a), so a female choosing a long-tailed male will be choosing a partner who will pass on a resistance to parasites to her offspring. The latter may then cope better with parasites while still in the nest and also be more attractive as mates later on. By mating with a parasite-free male, the female and her offspring may also avoid being infected directly themselves, although the importance of this is not clear (Møller 1991b). The number of mites in the nest by the time the first brood fledges is related to the number on the adults when they arrive, so it would be beneficial to avoid heavily infested males (Møller 1990a, 1991b). Avoiding parasites, and thus infested males, is important because parasites can impair the growth and chances of survival of young Barn Swallows (Chapter 8). By mating with a good-quality male, a female thus gets both a direct benefit of avoiding parasites for herself and her offspring and an indirect benefit of having offspring with high parasite resistance (Møller 1994a). However, the benefits of choosing parasite-free males can vary over time. Møller assessed the parasite status of his Danish population during the 1980s and 1990s and found that mites were scarcer and had less effect on fledgling production during the 1990s (Møller 2002b). In addition, the relation between tail length and mite infestation weakened and had disappeared by 1999. During the study, the average tail

14639.qxd

24/1/06

74

3:53 pm

Page 74

The Barn Swallow

Figure 4.2. The offspring of long-tailed male Barn Swallows have few parasites and are long-lived. Tail length of males is (a) negatively related to the number of blood-sucking mites on their offspring (fostered to another pair to avoid their parents infecting them) and (b) positively related to the longevity of their offspring. After Møller 1990b, 1994g. Copyright (1994) National Academy of Sciences, U.S.A.

length of males also increased at the same time as mites became less prevalent. Møller concluded that this population of Barn Swallows has become more resistant to these mites, perhaps through a reduction in the mites’ ability to feed on the birds’ blood, since fewer mites contained blood from a recent meal in 1999 than in 1988. Møller suggested that resistance to the mites increased at the same time as the males’ tail length increased because the two traits are genetically linked, and thus the mites became scarcer and less damaging to breeding success. However, the mites may eventually overcome this resistance and become more virulent again (Møller 2002b). In addition, Barn Swallows have many kinds of parasites (Chapter 9) and some of these

14639.qxd

24/1/06

3:53 pm

Page 75

Attracting and choosing a mate

75

may still affect the condition of adults and chicks and thereby influence the female’s mate choice. As well as being parasite-resistant, males with long tails are also more likely to survive from one breeding season to the next (Møller 1991k, 1994c; Thompson 1992; Saino et al. 1997b). There may be several reasons for their better survival, the main one probably being their more efficient immune system (Saino et al. 1997b). In the autumn, long-tailed males have larger fat stores than do short-tailed males, so they may be better able to survive a long journey if feeding conditions are poor (Rubolini & Schiavi 2002); they are also able to return earlier in springs with inclement weather than are short-tailed males (Møller 1994a,f ). A study of prey remains at 29 Eurasian Sparrowhawks’ nests found that long-tailed males were less likely to be preyed on than were males with short tails (Møller & Nielsen 1997). In addition, long-tailed males, at least in Europe, are better at surviving adverse weather: during a severe cold spell in the spring of 1987, the seven males in Møller’s study population that survived had significantly longer tails than the 22 that were found dead (Møller 1994f ). The offspring of long-tailed males have good survival prospects (Møller 1994g; Figure 4.2b); females mating with long-tailed males therefore provide their offspring with genes for viability, as well as good health. In contrast, Brown & Brown (1999b) did not find that long-tailed North American males survived better during a cold, wet period. Another indicator of the males’ health is the date they arrive back at the breeding grounds. Arrival dates of males are variable and it is likely that only the birds that are in good body condition will be able to arrive early and start breeding early; in turn they will have time for more than one brood and sire lots of fledglings (Thompson 1992; Møller 1994a; Ninni et al. 2004; Møller et al. 2004b). Early breeders are in better condition on arrival than those that arrive and breed late; they are heavier for their size (Møller et al. 2003; Ninni et al. 2004) and they have low blood leukocyte levels (indicating for example a lack of parasite infection, Pap 2002) and a high haematocrit (Ninni et al. 2004). Early males also have a good immune response and few harmful parasites (Møller et al. 2004b). Although body condition varies between years, and in favourable springs with a good food supply many males may be in good condition, those arriving early are still in better condition than later ones (Ninni et al. 2004). Females choosing males that arrive early are therefore likely to be choosing males in good condition. Fathers that arrive early have sons that do the same (Møller 2001a). Early males are also generally long-tailed ones, and long-tailed fathers have sons that arrive early and vice versa. However, males are still flexible and an individual will arrive earlier in a favourable spring than in a poor one (Ninni et al. 2004). Both tail length and arrival date reflect body condition; for example, for males of a given tail length, those in better condition will still arrive earlier (Møller et al. 2004b), and in favourable springs there may be little relation between the males’ tail lengths and when they arrive (Ninni et al. 2004). Winter feeding conditions are also important, allowing males to grow longer tails and long-tailed males to arrive earlier when the conditions are good (Saino et al. 2004a,c).

14639.qxd

24/1/06

76

3:53 pm

Page 76

The Barn Swallow

A male’s song and rate of singing also provide information to females about his age, parasite resistance and health (Chapter 3). Females may want to avoid firstyear males because they are generally less experienced and less able to defend the nest against intruders (Møller 1994a). Song is a better guide to age than tail length is, as the latter does not increase every year and even decreases in very old males (Chapter 1). When more than one male is singing, females may also be able to tell their relative quality by comparing their songs and seeing which male wins singing contests (Chapter 3). Møller et al. (1998a) suggested that a behavioural display such as singing, which may vary from day to day, is a less reliable guide to the overall quality of a male than a morphological one such as tail length and so females should give more weight to the latter when choosing a mate. Nevertheless, singing still provides some information about the current health of a male, as well as his age, and so is a particularly useful adjunct to tail length when females choose a copulation partner other than their own mate (Møller et al. 1998a; Chapter 5). From the male’s point of view, singing provides more flexibility in signalling to the female, whereas he is stuck during the breeding season with the tail that grew in the winter quarters. Singing may be a less honest signal of his quality which, at least in the short term, he can maintain to some extent regardless of changes in other signals (Saino et al. 2003f ). Thus a female has a variety of ways to assess the suitability of a male: morphological characters which provide a long-term view of his quality and his singing which indicates his age and health. These characters are correlated with each other, so that a long-tailed male also has a symmetrical tail and large white spots with little evidence of damage by parasites, but they have an independent influence on the female’s choice of a mate. There may be some geographical variation in the relative importance of tail length and other plumage features in mate choice. European females are clearly attracted to males with long tails, and benefit accordingly. Whether this is also the case in North America is not clear. In New York State, more colourful males, particularly with colourful bellies and vents, rather than males with long, symmetrical tails, had greater breeding success over a season (Safran & McGraw 2004). In contrast, in Ontario, in a study that also considered extra-pair offspring, long-tailed males were more successful (Kleven et al., in press b). In theory, North American males may experience less intense selection for long tails because, unlike their European counterparts, they share in incubation and a long tail may be damaged in the nest or the aerodynamic costs may be too high (Smith & Montgomerie 1991; Chapter 2). To what extent North American females prefer colourful males or long-tailed males is not known, however; the extensive experimental evidence on mate choice that has been obtained for European Barn Swallows is not yet available for those from North America. Tail length, and the length of the males’ tails in relation to those of the females, increases with increasing latitude (Chapter 1). Hence male Barn Swallows in southern Europe have relatively short tails, which is thought to be because of high foraging costs (Chapter 2), and thus selection for long tails may also be weaker here than in northern populations (Møller et al. 2003).

14639.qxd

24/1/06

3:53 pm

Page 77

Attracting and choosing a mate

77

THE COSTS OF BEING ATTRACTIVE Not all males can grow long tails and thus attract females; only those in good condition can do so. Thus males who suffer mite infestations of their nests when breeding are less able to increase the length of their tails over the next winter (Møller 1990b, 1991b). Even when rain is plentiful on the wintering grounds, providing ideal feeding, and hence moulting, conditions, males with short tails during the breeding season do not grow new tail feathers as long as those of long-tailed males (Møller 1991d, 1994a). A study of the length of daily growth bars in tail feathers (a result of differential growth during the day and at night) also found that long-tailed males grew their feathers more quickly than short-tailed males (Møller 1994a). This is despite having less time available for moulting, as they leave the breeding grounds later, after rearing two or three broods, and return earlier. Growing a new tail feather is more difficult during the breeding season, but, as Møller (1994a) showed by plucking tail feathers early in the season, originally short-tailed males also regrew shorter tails than their long-tailed counterparts. Short-tailed males also have poor-quality feathers. They are more likely to have fault bars (found in over 20% of males with the shortest tails and less than 10% of the longest-tailed males) and damaged tail feathers (found in over 10% of males with the shortest tails and none of the longest-tailed males, Møller 1994a) at the beginning of the breeding season. Fault bars are characteristic of nutrient or energy deficiency during moult and make the feather prone to breakage. Short-tailed males also have more holes in the feathers, probably caused by lice (Møller 1991b; Pap et al. 2005). Similarly, not all males can grow symmetrical tails. The level of asymmetry in the tail appears to be related to how well males cope with stressful conditions. In experiments, the asymmetry in tail length in one breeding season was correlated with subsequent changes in asymmetry over the next winter after a period of stress, such as an increase in parasite load or having to grow the outer tail feathers during the breeding season after the experimenters removed them (Shykoff & Møller 1999). Some males were able to maintain the level of symmetry in the tail despite difficult conditions, whereas others were not. The former seemed to be the better-quality males, as they also had more offspring than males that became more asymmetric. In an experiment, males stressed by having mites added to their nests grew the most asymmetric tails and those with fumigated and hence mite-free nests grew the least asymmetric tails (Møller 1992a). However, males with long tails were affected less than short-tailed males, suggesting that they coped better with the stress. Although attractive, long tails could be disadvantageous to males. They require extra resources to grow and, once grown, may affect flight (Chapter 2) and mortality, for example by making the birds more conspicuous to predators and less manoeuvrable when trying to escape from them. Experiments in which the tail is artificially shortened or lengthened have revealed a number of such disadvantages but they, and other evidence, also suggest that naturally long-tailed males are better able to cope with the costs of having a longer tail than naturally short-tailed males, indicating

14639.qxd

24/1/06

3:53 pm

78

Page 78

The Barn Swallow

their better condition. Similarly, males with other attractive features such as large tail spots are better equipped to cope with the costs than are less attractive males.

Flight costs Long tails, even natural ones, may reduce manoeuvrability or increase the costs of flying (Chapter 2). Thus, males fall prey to Eurasion Sparrowhawks more than the shorter-tailed females do (Møller & Nielsen 1997). Elongating males’ tails experimentally apparently makes it more difficult for them to catch large insects as they then bring relatively smaller insects to their chicks (Chapter 2). However, males with naturally long tails can capture larger prey than short-tailed males (Møller et al. 1995a). Males with elongated tails in Møller’s (1989c) study also grew shorter tails the following winter, whereas those with shortened or unaltered tails grew longer ones. More than three-quarters of males with elongated tails developed fault bars in their new tail and wing feathers, whereas the other males rarely did. The experiment thus suggested that males with artificially elongated tails were under more stress, perhaps because of increased flying or other costs. Perhaps as a consequence of their shorter tails with more fault bars, making them unattractive to females, the males whose tails had been elongated in Møller’s (1989c) study, compared with males with shortened tails, took longer to find mates in the next breeding season (8.5 days versus 2.6 days); although they eventually mated, they seemed to get only poor-quality mates, as only a quarter had second broods (versus 64%) and they reared an average of only four fledglings (versus 7.3).

Survival costs Although males with naturally long tails are generally healthy birds with good prospects of survival, the chances of survival of males given longer tails in experiments are generally reduced by about 8% and for males with shortened tails they are increased by about the same amount, suggesting that long tails are a liability (Møller 1994a; Møller & de Lope 1994; Saino et al. 1997b). Møller (1989c) did not find a significant effect of changing tail length on survival rate, but males with elongated tails that survived had longer tails initially, suggesting that they were better able to bear the extra costs. In Møller & de Lope’s experiment on Barn Swallows in Denmark and Spain, the survival rate of males with elongated tails was only 29% compared with about 40% for other males and 49% for males with shortened tails; in addition those males that survived had natural tails that were longer than those of males that did not, as in Møller’s (1989c) experiment, while males with a naturally short tail benefited from a shorter one. An elongated tail may thus be relatively more costly for naturally short-tailed males and even the natural tail length may be costly especially for short-tailed males (Møller 1994a; Møller & de Lope 1994). In addition, in the Danish study population, Møller & Szép (2002) found that survival rates of males were low when males in the previous breeding season had long tails on average. A natural increase in the tail length may thus increase the costs for males with consequences for their viability (Møller & Szép 2002).

14639.qxd

24/1/06

3:53 pm

Page 79

Attracting and choosing a mate

79

Health costs Males with artificially elongated tails have comparatively high haematocrit levels compared with unaltered males and males with shortened tails, suggesting that they need more energy and require more oxygen (Saino et al. 1997d). Saino et al. (1997c) found that long-tailed males in three populations (Denmark, Spain and Italy) had higher haematocrit levels when they arrived on the breeding grounds than shortertailed males and females. Haematocrit also declines from pre-laying to chick-rearing for males (Saino et al. 1997c; Pap 2002). The high haematocrit and its decline over the season may reflect the high cost of migrating and displaying to males with long tails (Saino et al. 1997c; Pap 2002). Compared with males with shortened tails and unaltered males, males with artificially lengthened tails produce only low concentrations of gammaglobulin, indicating a weak immune response, that is, imposing long tails on males seems to make their immune systems less efficient (Saino & Møller 1996). Only good-quality males with naturally long tails overcome this cost and still have an efficient immune system and high viability (Saino & Møller 1996). Males with long and symmetrical tails have high levels of the male hormone testosterone (Saino & Møller 1994), which is thought to depress the immune system and might thus make the bird more susceptible to infections and parasites. Although the intensity of parasite infestation is not related to naturally occurring testosterone levels (Saino & Møller 1994), males implanted with extra testosterone suffered higher infestations of feather lice; however, long-tailed males in this experiment had fewer lice than shorter-tailed males (Saino et al. 1995). The testosterone implants also reduced the males’ survival to the next breeding season, but survival was still better for long-tailed males. These males thus seem better able to cope with any adverse effects of the hormone. Why long-tailed males have high levels of testosterone is not clear; it may be a consequence of being involved in frequent chases and fights, as aggression can increase hormone levels (Hillgarth & Wingfield 1997). High testosterone levels are also associated with high levels of mate-guarding and sexual activity and with a reduction in parental care (Saino & Møller 1995a, b) and the mates of long-tailed males have high levels of testosterone in their eggs (Gil et al. 2005). Whether long-tailed males are disadvantaged in terms of energy expenditure is not clear. When Cuervo et al. (1996a) changed the tail lengths of Spanish males and females and measured their daily energy expenditure they found no effect of the manipulations. However, in another study in Scotland (A. Hill, unpubl. data cited in Buchanan & Evans 2001), in which the streamers rather than the basal parts of the tail feathers were reduced, both very short and very long reductions increased expenditure. Also in Scotland, Nudds & Spencer (2004) found an n-shaped relation between tail length and daily energy expenditure for males with their natural tail length, with males that had an intermediate length of 119 mm having the highest expenditure.

14639.qxd

24/1/06

3:53 pm

80

Page 80

The Barn Swallow

Other costs The white spots in the tail are weaker and more prone to breakage and wear than the black parts of the feathers (Kose & Møller 1999). They thus make an easy meal for feather lice, which preferentially attack the white areas of the tail feathers; this can lead to the tail breaking (Kose & Møller 1999; Kose et al. 1999). However, longtailed males suffer less damage from lice than short-tailed males, despite having a larger white area, again showing their superior quality (Kose & Møller 1999). Poorquality males cannot display tails with large areas of white because they would suffer from lice. Whether the red parts of the plumage are also costly to males is not known. The red coloration is based on melanin, with particularly high concentrations in the throat feathers (McGraw et al. 2004a, b). There may be a trade-off between using certain nutrients for coloration and other metabolic requirements, so that only good-quality individuals can afford to divert some of the nutrients from their food to develop bright plumage and still remain healthy. Whether the level of melanin in feathers, which is synthesised directly from amino-acids, reflects the quality of the individuals requires further research. Stressful events are thought to affect the development of signals such as tail symmetry differentially in good-quality and poor-quality males. Good-quality males may be able to overcome the stress and still express the signal, whereas poor-quality males cannot. In extreme circumstances, however, males in general may be unable to maintain signs of health. In the Chernobyl area, where Barn Swallows have been exposed to high radiation levels from the nuclear accident in 1986, their red colour is less intense and is not correlated significantly with tail length (Camplani et al. 1999). Chernobyl males also more frequently have white feathers in these red facial areas (Møller & Mousseau 2001) and have more asymmetric tails, and sometimes aberrant development of the tail, than before the accident and than in other areas (Møller 1993b).

ATTRACTIVE MALES AND PARENTAL CARE Another way of attracting females might be for males to show them that they would be willing and able to help rear the chicks. This is not the case for Barn Swallows: some studies have found that the attractive, long-tailed, symmetrical males can in fact make bad parents. Naturally short-tailed males take a larger share in feeding chicks than long-tailed ones: females with long-tailed mates contribute nearly 60% of feeds to chicks, whereas the shortest-tailed males and their mates feed them about equally (Møller 1992b, 1994a). Why long-tailed males should feed chicks at a lower rate is not clear, but they may be less efficient foragers. Møller (1994d) investigated this difference in feeding rates experimentally by increasing or reducing the length and symmetry of the tails of males. Males with long, symmetrical tails fed their chicks less frequently, both absolutely and relative to their partner, than

14639.qxd

24/1/06

3:53 pm

Page 81

Attracting and choosing a mate

81

those with short, asymmetrical tails, and their partners fed at a higher rate than partners of the latter. Tail length and symmetry both had an effect. The females compensated so that the overall feeding rate did not depend on the males’ tail length and symmetry. However, experimental manipulation of tail length does not always lead to a change in feeding rates of males, and females do not always compensate for the low feeding rates of their partners (Møller 1989c; J.J. Cuervo & A.P. Møller, unpubl. data). In another experiment in which tail length of males was manipulated after the female had chosen her mate, females mated to males with elongated tails not only fed the brood more but were also more likely to have a second brood (rearing an average of 2.1 broods versus 1.6 for those with short-tailed partners) and had more offspring (de Lope & Møller 1993b; Møller & de Lope 1995). However, this short-term investment may have long-term costs. Cuervo et al. (2003) found that females mated to long-tailed males produced relatively fewer chicks the following year than those mated to short-tailed males. Females mated to long-tailed males may thus do more work feeding the chicks and invest more in second broods than those with short-tailed mates. These females also do more nest-building, and more nest-guarding, although not more nest defence (Chapters 6, 8). In addition, they invest more in producing high-quality eggs with high levels of androgens and antibodies (Chapter 7). This difference in investment based on the partner’s quality could be because those females that mate with long-tailed males are of high quality themselves and able to work harder. Alternatively, these females could be willing to invest more in rearing offspring of attractive mates (the differential allocation hypothesis; Burley 1986; Sheldon 2000): if they have a high-quality partner, their offspring will also be of high quality, inheriting their father’s attractiveness, resistance to parasites and viability, and so be worth the extra commitment (Møller 1994d). The results of the tail manipulation experiments are consistent with this idea, that females adjust their parental investment according to the quality of their mate. Females also choose long-tailed males as extra-pair partners when they get no help at all from them. Females do not seem to benefit directly from having a long-tailed mate in other respects either. Long-tailed males are not less likely to be partially or totally infertile, for example; nor do they have better territories (Møller 1994a). Once a male and female have formed a pair, there is still opportunity for assessment of partners. A female may adjust her investment in a clutch depending on the level of investment by her partner. Soler et al. (1998) suggested that the female may do this by taking into account how much nest-building the male does. A male that spends time and effort on building may indicate that he is willing to invest a lot in feeding the brood (Møller 1994a). A female with a long-tailed mate will not get much parental help from him, but a female with a short-tailed mate who is willing to invest a lot in their offspring can still afford to lay more eggs than a female with a short-tailed mate that does little to help (Soler et al. 1998). Hence a female’s preferences and investment depend on the male’s breeding strategy (Qvarnström et al. 2000).

14639.qxd

24/1/06

3:53 pm

Page 82

82

The Barn Swallow

MALE MATE CHOICE Females vary markedly less than males not only in tail length but also, for example, in arrival date and mating and breeding success. These characteristics are also less dependent on the condition of the bird in females than in males. Tail length and arrival date of females are not related to measures of health such as intensity of parasitism or immunocompetence (e.g. Møller 1994a; Saino et al. 1997b, 2002d; Møller et al. 2004b). This low variability and condition dependence is presumably because females are not under such intense selection as males, which need to arrive early and be healthy and attractive to females, as both social and extra-pair mates, to maximise their fledgling production. Nevertheless, long-tailed females are still heavier and in better condition than short-tailed ones (Møller 1992b). In Møller’s (1993c, 1994a) study, long-tailed females started breeding earlier and were more likely to have a second clutch, and therefore more fledglings during the season, although they did not have larger first clutches than short-tailed females. In addition, females’ clutch and brood sizes, and the likelihood of having a second clutch, increased between years as tail length increased with age. Thompson (1992) also found that longer-tailed females in Scotland started to lay early. Tail length, before or after manipulation, had no effect on the number of clutches or eggs or on fledging success in a Spanish population, however (Cuervo et al. 1996b; Møller et al. 2003). The following year, females with artificially elongated tails produced relatively fewer chicks than females with shortened or unaltered tails, showing a long-term cost to having a long tail (Cuervo et al. 2003). Cuervo et al. (1996b) also found no effect of the female’s tail length on feeding rates to chicks, but Møller (1993k, 1994a) did find that long-tailed females that had two broods fed at a higher rate. In addition, females with symmetrical tails lay sooner than those with asymmetrical ones (Møller 1994a). In Safran & McGraw’s (2004) study in North America, it was the females with the more colourful breasts and bellies, not those with long tails, that laid earliest, had more than one brood and fledged the most offspring. Tail length in individual females was not related to their survival in the Spanish population or in an early study in Denmark (Møller 1991c; Cuervo et al. 2003). However, Brown & Brown (1999b) found that long-tailed females in North America were more likely to survive a period of cold, wet weather, so such females may have an advantage in particularly adverse conditions. In a recent analysis of recaptures of Barn Swallows in the Danish study population, Møller & Szép (2002) found that female survival was better when females on average had long tails and high weights. The evidence thus points to tail length in females reflecting their body condition and it may not depend on the birds’ inherent quality as much as it appears to in males. Thus, for example, it is less affected by age and is not related to feather growth or the frequency of fault bars (Møller 1994a). Males do not choose long-tailed females as mates: in their tail manipulation experiment, Cuervo et al. (1996b) found that Spanish females with elongated tails

14639.qxd

24/1/06

3:53 pm

Page 83

Attracting and choosing a mate

83

did not mate earlier. Long-tailed females arrive first at the breeding grounds and this may account for long-tailed males tending to mate with long-tailed females rather than males preferring them (Banbura ´ 1986; Thompson 1992; Møller 1994a; Cuervo et al. 1996b). In a North American study, males and females of a pair were similar in throat and breast colour, rather than in tail length (Safran & McGraw 2004). It is not known whether colourful North American females are also those in good condition; colourful birds may pair up because they arrive on the breeding grounds at the same time rather than because of a preference. Long-tailed males may not judge females by their tails but they do get goodquality females as mates, at least in terms of body weight and prospects of survival (Møller 1991l, 1992b). This was evident in studies of males with natural and with manipulated tail lengths. As well as surviving better than females mated to shorttailed males, females with long-tailed mates also breed more quickly after mating, have larger broods, are more likely to have second broods, and fledge their second broods more quickly (Møller 1991l, 1992b; de Lope & Møller 1993b; Møller & de Lope 1995; Saino et al. 2004c). In addition, the high chances of survival mean that the pairs are more likely to be together in subsequent years. This is an advantage as such pairs start breeding sooner and rear more fledglings than pairs of birds that individually have breeding experience but that have not bred together before (Møller 1991l). The high breeding success of pairs with long-tailed males seems to be mainly the result of their early start rather than the females being larger or older (Møller 1992b). Thompson (1992) also found that longer-tailed males in Scotland started breeding early; although they did not have more fledglings over the whole breeding season, they had more from the first brood and hence their offspring had a higher chance of recruiting into the population (Chapter 10). Finally, long-tailed males benefit by having mates that take on a relatively greater share of the parental care and invest more in their offspring.

14639.qxd

24/1/06

3:53 pm

Page 84

CHAPTER 5

Breeding strategies They are undoubtedly the most nimble of all the species; and when the male pursues the female in amorous chases, they then go beyond their usual speed, and exert a rapidity almost too quick for the eye to follow. Gilbert White, 1789

Barn Swallows are socially monogamous, with pairs rearing broods together and often staying together for subsequent broods and in successive years. Occasionally a male will have two mates, while others remain unmated. However, although they breed as pairs, both males and females adopt other breeding strategies such as engaging in extra-pair copulations, that is, copulations with individuals other than their social mates.

14639.qxd

24/1/06

3:53 pm

Page 85

Breeding strategies

85

PROMISCUITY AND CUCKOLDRY To be successful in evolutionary terms, male Barn Swallows need to father as many offspring as possible, that is, to pass on as many copies of their genes as they can. This means being promiscuous rather than settling for the few offspring that they could sire with a single mate. Females are limited in the number of offspring they can produce, but they can ensure they have as many of the best-quality ones as they can, those most likely to recruit into the breeding population. They, too, can do this through promiscuity. As well as mated individuals looking for extra-pair partners in a breeding group, there are also those that do not get a mate straight away. An excess of males over females in breeding groups has often been recorded, both in North America and Europe (e.g. 13% in Kansas, Anthony & Ely 1976; 13% in Denmark, Møller 1994a; 8–9% in Germany, Loske 1994; Brombach 2004). Many of these males are first-years, but a group may also have more old males than old females (Saino et al. 2003d; Brombach 2004). In contrast, females usually start breeding the year after hatching. In Møller’s (2004a) study, the percentage of unmated males varied over 25 years from about 2% to 19%. The population declined over this period and unmated males became relatively uncommon when numbers were low. The excess of males at breeding sites creates the potential for intense competition between them for both nest sites and females. This is particularly so in large groups, where there is a greater proportion of unmated males than in small groups, possibly because these males are attracted to places where there are potential extra-pair mating opportunities (Møller 1988b). A conspicuous feature of a breeding site, especially early in the season, is the frequent chases between Barn Swallows, in and around the buildings where the nests are. These are more common where the Barn Swallows are breeding in groups, although solitary pairs are sometimes visited by outsiders. A female is often chased by a male other than her mate, intent on copulating with her. In turn, the intruder is chased by the female’s mate, if present, and in the vast majority of cases he will be close by (see below). It is the male that takes the initiative, approaching a female, especially when her partner is not watching (Møller 1985). He rapidly utters the copulation call while hovering above the female. The female has the final say, though, and may attack the male or fly away if she does not want him. The male attempting the extra-pair copulation is usually the female’s immediate neighbour (in two-thirds of cases in the study by Møller 1985) or from up to four territories away, but males from outside the group can also father offspring by extra-pair copulations. Both chases and attempts at copulating outside the pair bond, unlike pair copulations, are most frequent during the female’s fertile period, although chases occur over an extended period, especially for first clutches (Møller 1985). A female is also most likely to accept another male during her fertile period. A male seeking extra-pair copulations tends to do so once his own mate has laid her eggs, that is, when she no

14639.qxd

24/1/06

86

3:53 pm

Page 86

The Barn Swallow

longer needs to be guarded (see below). Extra-pair copulations comprise about 10% of all copulations (Møller 1985, 1987f, 1994a) and usually occur later in the morning than pair copulations (Møller 1987f ). Møller (1985) found that as many extrapair copulation attempts led to copulations (24%) as did those between pair members (23%); the former may be more likely to result in offspring, however, because in birds the last male to copulate with a female tends to father relatively more of her offspring (Birkhead & Møller 1992). Both males and females use extra-pair copulations as a strategy to improve their breeding success. Males can help their partners rear one set of chicks while also fathering chicks in other nests. Females could improve the quality of their chicks by mating with males that are superior in some way to their partners; this would be especially useful for those females who arrive too late to mate with the best males – who have already been chosen as mates by earlier females – and have had to make do with poorer ones. Females should thus be choosy about which males they accept as extra-pair mates. Møller (1992b) found that females whose mates had short tails accepted extra-pair copulations, whereas those with the preferred long-tailed males did not. In an experiment, females mated to males with artificially elongated tails also did not copulate outside the pair bond, whereas those with mates whose tails were shortened did (Møller 1988a). Saino et al. (2003g) have shown that mating with long-tailed extra-pair males is a successful strategy for females with short-tailed partners, because they thereby have sons that grow up to have longer tails than their foster fathers. Males who breed early and females who breed late are the ones most involved in extra-pair copulations (Møller 1985). Because there is often a wide spread in laying dates within a group of Barn Swallows, early males can start one family, guarding their mates when they are fertile, and then copulate with other females when their own mates are incubating. Males guarding their mates can also be on the look-out for an opportunity to copulate with their neighbours (Møller 1985). Pairs seem to be consistent in the frequency of extra-pair (i.e. illegitimate) chicks in their successive broods, suggesting that females are consistent in whether they accept other males as copulation partners (Møller & Tegelström 1997; Møller et al. 2003). Females do not seem to get any other benefits from copulating outside the pair bond, such as more fertile sperm or parental help (Møller 1994a). Unpaired males would also benefit from mating with paired females, but are unlikely to be successful if they try. Females prefer already mated males, especially those with long tails and few parasites, as extra-pair copulation partners (Møller 1988a,b, 1991b, 1992b). Long-tailed males are thus more successful at getting extrapair copulations, as well as at attracting mates, than short-tailed males; successful males are also likely to be neighbours of the females (Møller 1985, 1992b). Only a few males manage to copulate with other females, and very few with more than one; most get no extra-pair copulations (Møller 1992b). Møller (1994a) found that no unmated males were successful at getting extra-pair copulations, usually because the females rejected them, whereas about a quarter of extra-pair copulation attempts by mated males appeared to succeed.

14639.qxd

24/1/06

3:53 pm

Page 87

Breeding strategies

87

Møller (1991e) found that whether males and females pursue extra-pair copulations depends on the size of the group they are in and also on the population density, as this affects group size and the spacing of nests and thus the availability of extra-pair partners (Chapter 3). A quarter of males and a third of females in groups are involved in extra-pair copulations and those in larger groups are more likely to be involved (Møller 1991e, 1994a). However, Safran (2005) found no relation between extra-pair paternity (that is, paternity resulting from extra-pair copulations) and group size in her North American population. Many chicks are the result of successful extra-pair copulations, as can be seen from DNA analyses, and a third to a half of broods contain at least one such extra-pair chick (Table 5.1). The frequency of extra-pair chicks in nests reflects the frequency of extra-pair copulations (Møller 1994a). First, second and third broods can have extra-pair chicks (Møller et al. 2003); extra-pair copulations are just as frequent for second as for first broods (Møller 1991i), and first and second broods of the same females have similar levels of extra-pair paternity (Møller & Tegelström 1997). In Spain, however, third broods had a lower frequency of extra-pair paternity (20%) than first (31%) or second broods (32%) (Møller et al. 2003). The fathers of the extra-pair offspring are often paired with females in the group and have their own broods (e.g. Saino et al. 1999c; Kleven et al., in press b). The frequency of extra-pair paternity varies geographically, with significantly fewer extra-pair chicks in Spain (Møller et al. 2003; Table 5.1). Møller et al. (2003) also recorded, in this population, cases where a male was the father of a chick in his own nest but his social mate was not its mother, indicating that another female had mated with him and laid an egg in his nest (this occurred in 2.6% of chicks and 2.9% of broods). The researchers suggested that this was due to the high density at which the pairs were nesting, with nests less than two metres apart. Other suggested explanations for these results, such as males rapidly switching mates (Griffith et al. 2004), can be excluded (A. P. Møller, pers. comm.). Table 5.1. Percentage of extra-pair chicks (chicks not sired by the female’s social mate) and percentage of broods with at least one extra-pair chick. % Chicks that are extra-pair

% Broods with extra-pair chicks

Number of chicks/broods

Locality

Source

29 31

45 50

45/11 391/86

Ontario, Canada Ontario, Canada

23 28

49 33

306/61 261/63

New York, USA Denmark

29 18

52 32

214/52 674/170

Italy Spain

Smith et al. 1991* Kleven et al., in press b Safran 2005 Møller & Tegelström 1997 Saino et al. 1999c Møller et al. 2003

* Part of an experimental study in which male tail length was manipulated.

14639.qxd

24/1/06

88

3:53 pm

Page 88

The Barn Swallow

Having one female as a partner and copulating with others can be a very successful strategy for those males able to attract females. In Spain, body condition was the most important factor determining extra-pair paternity; it may affect a male’s attractiveness to females via his ability to sing and display, as well as how early he can return from the winter quarters and thus how soon he can start breeding (Møller et al. 2003). A female looking for a good-quality male as a father would do well to get one in good condition; however, a female cannot easily assess a male’s body condition or even arrival date (since males arrive before females), but she may use tail length as a surrogate indicator of the quality of potential extra-pair mates, as she does when choosing a longer-term partner (Møller et al. 2003). Long-tailed males are not only more likely to get extra-pair copulations, but they are also less likely to have other males’ chicks in their own nests, perhaps because they can protect their paternity or because their mates already have good-quality partners and do not desire copulations with other males (Møller & Tegelström 1997; Møller et al. 2003; Chapter 4). Saino et al. (2003g) found that long-tailed males were less likely to have such ‘foster’ sons recruiting into the population. In a study of Italian Barn Swallows, naturally long-tailed males fathered more chicks than did shorttailed males both in their own nests and in the nests of other males: some long-tailed males had as many as 12 biological offspring compared to none or at most four or five managed by short-tailed males (Saino et al. 1997e). Males with artificially elongated tails also fathered more offspring in their own nests and in total, whereas males whose tails were shortened had the lowest paternity, with other males being intermediate (Figure 5.1). Females’ extra-pair partners had longer tails than the females’ own mates (Saino et al. 1997e). Long-tailed males may have an additional advantage, as tail length is correlated with testes size, so they may deliver more sperm than shorter-tailed males in extra-pair copulations, and hence have a greater chance

Figure 5.1. Male Barn Swallows with artificially lengthened tails have more offspring in their own and other broods than males with shortened or unaltered tails. (Controls: feathers cut and re-glued or left unaltered.) Vertical lines represent standard errors of the mean. From Saino et al. 1997e.

14639.qxd

24/1/06

3:53 pm

Breeding strategies

Page 89

89

of fertilising the females’ eggs (Møller 1994a). Besides tail length, the males’ song rates also affect their paternity: singing at a high rate is associated with high paternity in the broods they help to rear (Møller et al. 1998a; Chapter 3). However, this relation is much weaker than that between male tail length and paternity. In Spain, however, tail length is only weakly related to the degree of extra-pair paternity, perhaps because the difference in tail length of males and females (about 5%) is smaller than that in Denmark and Italy (about 12%; Møller et al. 2003). Having extra-pair partners here may also be of less value than elsewhere, because young birds tend to breed close to where they were hatched in this population, so inbreeding may reduce genetic variation between males and hence the benefits of mating outside the pair bond (Møller et al. 2003). In Canadian studies, the likelihood of being cuckolded was also not consistently related to tail length (Smith et al. 1991; Kleven et al., in press b). In contrast, the ventral coloration of North American males influences their risk of being cuckolded; Safran and her colleagues in New York State found that males whose underparts were experimentally painted a darker red were less likely than less colourful males to lose paternity in successive breeding attempts with their social mates (Safran et al. 2005). The level of extra-pair paternity in a population probably depends on how synchronously the pairs are breeding (Saino et al. 1999c). Males that mate outside the pair bond often do so with neighbouring females and at times when their own females are not ready to lay but other females are. Males are less likely to be cuckolded when the group is breeding synchronously, when fewer males may be able to leave their own females to mate outside the pair bond. Male tail length correlates negatively with breeding asynchrony within a group, and Saino et al. (1999c) suggested that this could be in part because females with low-quality, short-tailed mates lay eggs when high-quality, long-tailed males are available for extra-pair mating, and so the females of the long-tailed males are not at the laying stage. Although both males and females can benefit by pursuing copulations outside the pair bond, there are potential disadvantages to this behaviour. Males that spend time away from the nest risk being cuckolded themselves, they may also be involved in potentially dangerous fights and be exposed to more diseases and parasites, and they may not have enough sperm left to mate with their own females. There is no evidence that these risks are serious, however, especially as males are generally not looking for extra-pair mates when their own mates are laying (Saino et al. 1999c). For females, there is also a risk of catching diseases and parasites and of having their own mates reduce their investment in the chicks if they are uncertain of their paternity. Some experiments and observations suggest that males will invest less in offspring that might not be their own, but it is not clear why they should do so, as they risk harming their own chicks. Møller (1988c, 1991h) found that males fed and defended chicks less after he experimentally increased the number of extra-pair copulations that their mates experienced. He caught and kept some group-living males captive for two hours early in the morning, allowing extra-pair copulations to take place. During the chick-rearing period, these males stayed further away and gave

14639.qxd

24/1/06

3:53 pm

Page 90

90

The Barn Swallow

fewer alarm calls in response to a model of an owl than males detained during incubation or in solitary pairs, indicating a low commitment to the brood. In a similar study, how often males in groups fed their broods was positively related to the number of copulations with their own females and negatively related to the number of chases and extra-pair copulations in which the females were involved (Møller 1988c). However, females also reduced their parental care and more chicks died in the experimental broods than in control ones, so the change in male behaviour could have resulted from the males having smaller broods (Wright 1992). Møller & Tegelström (1997) found no relation between male feeding rates and whether the pairs had extra-pair chicks, although for six pairs with different levels of extra-pair paternity in first and second broods, the males fed the brood less when the frequency of extra-pair paternity was higher. However, males feed their own and extra-pair chicks within a brood the same amount, thus apparently not discriminating between them (Møller et al. 2004a).

MATE-GUARDING Because of the risk of extra-pair copulations, a male guards his mate, staying within five metres of her, from three weeks before she starts laying until the start of incubation (Møller 1987a, 1994a; Saino et al. 1999c). He spends about three-quarters of his time in her presence (Møller 1994a). The time that a male spends near his mate increases to a maximum before she starts laying and gradually declines during egg-laying and incubation (Møller 1985, 1987a; Saino & Møller 1995a; Saino et al. 1999c). The male is at less risk of being cuckolded as more eggs are laid, because the female spends more time on the nest and fewer eggs are left to be fertilised. If the pair go on to have a second brood, the male guards her as much during her second fertile period as during her first (Møller 1991i). The period over which males guard and how much time they spend guarding are related to the risks of being cuckolded. Thus males spend more of their time guarding their females in larger groups (Møller 1987a, d). Males in groups also start guarding earlier in the females’ nesting cycle and guard more and for longer when the sex ratio is skewed towards males (Møller 1987a). Males with fertile females will also guard more when chases are frequent in a group (Møller 1987e). Males within five metres of their mates always see off other males, either chasing them or interfering with an attempt at copulation (Møller 1985) and, if males are temporarily removed, their mates are chased and extra-pair copulations are more frequent (Møller 1987e). When the males are absent (about 12% of chases), about half the chases lead to extra-pair copulations. When they chase off intruders, males may do so silently or utter an alarm call, which puts other Barn Swallows to flight and so may disrupt the intruders’ attempts at copulation (Møller 1985). However, the frequency of extra-pair copulations does not depend on how much guarding males do (Møller 1994a), and Møller & Tegelström (1997) found that males with

14639.qxd

24/1/06

3:53 pm

Breeding strategies

Page 91

91

and without other males’ chicks in their own nests both spent about 75% of the time guarding their mates, so the effectiveness of mate-guarding is not clear. In addition to protecting his own paternity, the male may also help his mate by preventing other Barn Swallows from harassing her. Without a male to guard her, a female can be chased at a high rate; for example Møller (1987e) recorded an average of 11.2 chases of females in two hours without a male and 2.4 chases in two hours when a male was present. The extended period during which copulations occur in groups may even be a ploy by females to persuade their mates to guard them before the fertile period; copulating with and following the male might make him unsure about whether she was ready to lay, so he would guard her in case she was (Møller 1985, 1987f ). Møller (1987a) also suggested that, during the egg-laying period, the female may be able to assess the quality of her mate by whether he is still able to guard her, and she may choose to copulate with another male if her mate fails her. Males may also use other means to protect their mate from males that are looking for extra-pair partners. They defend a larger territory during their mate’s fertile period (for both clutches) than later during incubation or chick-rearing (Møller 1990e; Chapter 3). They also sing at a high rate at this time, which may deter intruders (Møller 1991m, 1994a; Saino et al. 1997a; Chapter 3), and they utter alarm calls if they lose contact with their partner (Møller 1990c). They often leave the female sitting on the nest during the egg-laying period, but return regularly and will usually fly around the breeding site, uttering alarm calls if they find the female absent. Although the same call is used if a predator is seen, in these cases males use alarm calls deceptively as no predator is present. Instead, Møller (1990c) found that this behaviour was related to the males’ risk of being cuckolded. Møller chased females from the nest and recorded the subsequent behaviour of their mates. Returning males uttered more alarm calls during the egg-laying stage than during nest-building or incubation, and more if they were breeding in groups than nesting solitarily. The presence of a mounted male Barn Swallow also induced alarm calling by both males breeding in groups and solitary ones. It is not clear how effective alarm calling is as a paternity guard, but Møller (1990c) recorded five attempts at extra-pair copulations being disrupted in this way. During their mate’s fertile period, a high copulation rate is itself probably a means for males to ensure that they are the fathers, because they may thereby dilute any sperm from other males and because they are more likely to be the last male to mate with the female and hence to fertilise the eggs. As added insurance, males copulate with their mates if the latter have been chased by other males, at least during their fertile period (Møller 1987f ). Males are unlikely to see their females engage in extrapair copulations because they chase off intruding males, but the frequency of chases may indicate how interested other males are in particular females and so how likely such copulations are (Møller 1988c). Pairs living in groups copulate more often than solitary pairs do, at average rates of 0.45 and 0.16 times an hour, respectively, perhaps because males in groups run a greater risk of being cuckolded (Møller 1985). Long-tailed males copulate more frequently, perhaps because they also have larger testes than short-tailed males and so may be able to copulate often without

14639.qxd

24/1/06

92

3:53 pm

Page 92

The Barn Swallow

depleting their sperm (Møller 1994a). As with mate-guarding, however, the effectiveness of frequent copulation as a means of preventing extra-pair copulations is not clear, as males with and without other males’ chicks in their nests have been recorded copulating at similar rates (Møller & Tegelström 1997). Individual males vary in how long and how intensely they guard their mates; some start late in their female’s nesting cycle or guard at low levels and fail to prevent her from mating with other males. Old, heavy males, however, guard until late in the female’s nesting cycle (Møller 1987a). How much males guard their mates is not strongly related to their tail length (Møller 1994a), but it is related to the level of the hormone testosterone in their blood. Mate-guarding peaks about a week before the hormone does and individuals with high levels also guard intensively (Saino & Møller 1995a). Although long-tailed males have high testosterone levels, they are not the ones that guard their mates the most: among males with similar testosterone levels, short-tailed males actually guard more intensively (Saino & Møller 1995a). This may be because the mates of long-tailed males may be unlikely to copulate with other, shorter-tailed males (Møller 1985, 1988c), so there is less need for these females to be guarded; furthermore, the long-tailed males may then be free to spend time copulating with other females (Saino & Møller 1995a). Although males may benefit from guarding their mates, there are drawbacks. Males so engaged have less time to feed themselves and, if they are following their female when foraging, may miss out on prey because their partner catches them first. Indeed, males lose weight during the guarding period (Møller 1991e; Birkhead & Møller 1992), and it is the heaviest males that can continue guarding the longest (Møller 1987a). Males that are guarding their own females are also unable to seek out other females for extra-pair copulations (Saino et al. 1999c). In addition, when both members of the pair are away, the nest is exposed to nest competitors and conspecific intruders (see below). Males may thus time their mate-guarding to the most critical period as far as possible. By removing or adding eggs to nests, Møller (1987e) showed that males respond to the behaviour of their mates; they guarded more when eggs were added and when females with reduced clutches spent more time away from the nest. Neighbouring males apparently also responded to the increased mate-guarding by chasing these females more.

OTHER BREEDING STRATEGIES Males Males sometimes pair with two females at the same time (e.g. Medvin et al. 1987; Cramp 1988; Saussay & Jacob 1993; Brombach 2004). Given the many intensive studies of Barn Swallows and the lack of reports of this happening, polygyny is apparently rare in most populations, although in Spain perhaps 1% of males are polygynous (A.P. Møller, pers. comm.) and 2% of males were polygynous in a Canadian colony in one year (O. Kleven, unpubl. data). It can happen when there

14639.qxd

24/1/06

3:53 pm

Breeding strategies

Page 93

93

are two more-or-less synchronous nests close enough to each other for a male to include both in his territory. The male may attract two females or acquire one of them if her mate disappears; he may even drive the latter away. Males may also be monogamous in one year and polygynous in another. In some cases, polygynous males help to look after both broods, but in others one of the broods is ignored. Although females will at least partially compensate for the absence of males (Chapter 8), this may be difficult for them in bad weather, so polygyny is probably not often likely to be a profitable strategy in terms of number of fledglings produced. Males that fail to acquire nest sites and attract mates stay on the lookout for mating opportunities, for example females that become available if their mate dies. Sometimes they create their own opportunities, by displacing other males and destroying their broods or, more usually, by killing the offspring of females whose own mate has disappeared. Females who lose their brood and partner will mate with the killer because at least then they will have a chance of rearing a brood successfully that season. Males benefit from killing the broods of widowed females, rather than waiting for them to fledge before mating, because they can sire their own broods more quickly. The earlier these males can breed the more fledglings they are likely to have. Nevertheless, they are likely to rear fewer fledglings than males that mated and bred earlier. Several instances of infanticide have been witnessed and many others inferred from the disappearance of young chicks (e.g. Crook & Shields 1985; Møller 1988b, 1994a, 2004a; Wellbourn 1993; Banbura ´ & Zielinski ´ 1995a). Males have been seen pecking chicks on the back and head and picking them up by the head and dropping them on the ground, one by one. Chicks are killed when only one to four days old; older chicks may be more difficult to remove from a nest but can still be attacked (e.g. Wellbourn 1993). Crook & Shields (1985) reported eight cases of infanticide out of 89 nests; four of the males re-nested with the victimised females and in three of these cases the brood’s father had already disappeared or died. Over 25 years, Møller (1988b, 1994a, 2004a) and his assistants directly observed 17 instances of males killing broods, and there was evidence of another 21 occasions (1.8% of nests); of the 17 that were witnessed, 11 were at nests where the males had already disappeared and in the remainder a male chased off the owner of the nest before destroying the chicks. Because they need time to re-nest, males kill only chicks of first broods; Møller and his colleagues recorded no cases of infanticide in second broods. Nests most at risk are first broods that are started relatively late. The risk of infanticide also increases with group size, because more unmated males are present (Møller 1988b). In a group of more than 50 nests in Nebraska, destruction of eggs and chicks by conspecifics was thought to be responsible for most of the high level of nest failures (78.3%, Hoskyn 1988 cited in Brown & Brown 1999a). At the other extreme, however, Thompson (1992) recorded no infanticide or eggs being removed in Scotland in groups of 1–14 pairs. Some males commit infanticide because they could not acquire mates by other means, but others resort to it after losing their own mates earlier in the season. In addition, males can be infanticidal one year and not the next or become

14639.qxd

24/1/06

94

3:53 pm

Page 94

The Barn Swallow

infanticidal after breeding successfully for a number of years (Crook & Shields 1985). Among unmated males, those that kill chicks are those with longer tails (i.e. the more attractive ones), whereas the fathers of the broods they victimise are relatively short-tailed males, which are probably paired with females that are not very efficient nest-guarders (Møller 1992b, 1994a). Victimised males are also younger than males at other nests and their clutches are started later (six days later on average, Møller 1992b, 1994a). Of 81 unmated males in Møller’s study, 23% acquired a mate by killing her chicks. The frequency of infanticide varies between years: from 0 to 5% of nests in Møller’s study (Møller 2004a). There are more cases when unmated males are relatively common, and when numbers of Barn Swallows, and hence competition between males, are high (Møller 2004a; Figure 5.2). Infanticide also depends on the ability of nest owners to guard and defend their nests and hence is more frequent when males in the population are in poor condition, with low weights (Møller 2004a). To find opportunities for infanticide, males need information about the breeding status of other individuals and, to get this, they often visit nests. Crook & Shields (1987) found that 16 of 17 frequent male visitors were unmated, the majority from the time they had arrived but four had lost mates; frequent nest visitors were also younger than other males. Møller (1988b) found that males visited an average of 2.1 nests (range 0–5). Sometimes visitors just perch near or on the nests, and sing or follow the females. They may chase the nest owners and try to copulate with the females

Figure 5.2. Infanticide is more frequent (a) when there are many unmated males in the population and (b) in large populations. Population size was set to index 100 in 2002. Reprinted from Møller, A.P. Rapid temporal change in frequency of infanticide in a passerine bird associated with change in population density and body condition. Behavioral Ecology (2004) 15(3): 462–468, by permission of the International Society for Behavioral Ecology.

14639.qxd

24/1/06

3:53 pm

Breeding strategies

Page 95

95

but they will also do apparently helpful things such as nest-building, mobbing predators, incubating eggs, and brooding and feeding chicks, perhaps to increase their chances of becoming the females’ mates for their next clutches (Crook & Shields 1985, 1987). In at least one case, a male adopted the chicks instead of killing them, helping to brood and feed them (Crook & Shields 1985). Although some visitors kill chicks, overall the behaviour of visitors does not affect the success of the nests they visit (Crook & Shields 1987). Many of the nests in a group will be visited by other Barn Swallows. In Crook & Shields’ (1987) study, 78% of nests were visited at least occasionally and 24% had frequent visitors. Visited nests typically had young male owners with partners older than the females in other nests. Nests were visited at all breeding stages but most often at the hatching stage, perhaps because visitors then are attempting to interrupt a breeding attempt by killing the young chicks. When the visitors were breeding males, the visits were mostly when the males’ partners were incubating; these males may be looking for extra-pair partners when their own mates no longer need guarding. As mentioned above, when infanticide occurs, the perpetrators may gain by mating with the female at the nest. Other visiting males may also benefit from their behaviour, however. Crook & Shields (1987) found that nine of ten males returned the following season to the cluster of nests they had visited, and in three of six instances when a visitor and the female he visited both returned, these birds paired with each other. Visitors may thus become familiar with the site, and with potential mates and competitors, improving their ability to get a nest and mate later on, and may also learn about the availability of individuals as partners when, for example, a nest fails or a divorce occurs (Crook & Shields 1987; Medvin et al. 1987). A well-guarded nest is at less risk from infanticidal males (Møller 1988b). Females spend more time than males guarding the nest, often being at the nest incubating eggs or brooding young chicks anyway while the males are collecting food. In addition, nests in groups, especially large ones, need more careful guarding than solitary ones because of the increased risk of other Barn Swallows intruding on them. Consequently, females in groups spend more time guarding than solitary females (73% versus 58% of the time; Møller 1988b). Males guard for about the same time regardless of whether they are in a group. Some females are better at guarding the nest than others, in particular those mated to long-tailed males (Møller 1994a). Other Barn Swallows are usually relatively easy to chase away, so are a threat only to poorly defended nests. For example, if a paired male with a young brood is killed by a predator, his mate will be unable both to brood and guard the chicks and to find food for them, allowing unmated males time to kill them. Møller (1988b) showed the importance of guarding experimentally by keeping males captive for a morning: in groups of Barn Swallows, guarding of broods aged one to five days fell from 86% of the time in nests with males present to 69% in those where males were absent, whereas for solitary pairs guarding time fell from 77% to 50%. Chicks were killed in four of the ten experimental group nests and not in other nests. Guarding was less intense at the victimised nests.

14639.qxd

24/1/06

96

3:53 pm

Page 96

The Barn Swallow

Females Female Barn Swallows sometimes lay eggs in the nests of other pairs, a practice known as brood parasitism or egg-dumping (Møller 1987c, 1994a). These parasitic females lay in the nests of close neighbours that are also at the egg-laying stage, as well as having clutches of their own. Females who have eggs dumped in their nests seem to fail to recognise the new egg, neither do they realise that two eggs have appeared in a single day; they just continue laying as normal. However, if eggs appear in the nest before the owners have started laying, they will eject them. The risk of throwing out their own eggs may be too great for females to locate and eject alien eggs, and the frequency of egg-dumping may be too low for recognition to evolve. In Møller’s (1987c, 1994a) study, egg-dumping was frequent with 13% of first broods and 22% of second broods being affected. It was also more common in large groups (none in groups of 1–4 and 25% in groups of 17–32) and when the population density was high. However, egg-dumping is variable between years and other studies report that it is rare. For example, less than 0.4% of offspring were attributable to egg-dumping in Saino et al.’s Italian population (Saino et al. 1997a, 2002f ). Nor was there evidence for it in studies in Scotland or North America (Thompson 1992; Brown & Brown 1999a; Ward & Bryant 2006; O. Kleven, unpubl. data; R. J. Safran, unpubl. data). Parasitic females benefit by having other females rear some of their chicks. They produce more offspring in each brood and over the whole season. In Møller’s study, they had an average of 5.8 fledged offspring in first broods and 5.1 in second broods, including those reared in other females’ nests; by comparison, their victims had only 3.1 of their own and the average for other females was 3.8. Guarding the nest is an effective deterrent to parasitic females and nest owners are usually at their nests early in the morning when parasitic females are looking for victims. Nevertheless, some nests are guarded better than others: Møller (1987c) found that it was the least well-defended nests that were parasitised. Møller (1989b) also investigated the importance of guarding by putting up old Barn Swallow nests containing eggs; these were used as host nests four times as often as active nests guarded by their owners. A study in North America found that Barn Swallows in a group of four pairs guarded their nests for only 29% of the time compared to 55–75% of the time for Møller’s Danish birds, perhaps because of the lower risk of egg-dumping (Brown & Brown 1996, 1999a). The risk of egg-dumping also depends on what the neighbours are doing. Parasitic females tend to use nests close to their own, but only if these are at the same breeding stage; a Barn Swallow’s nest close to one at an earlier stage is at less risk, both because that neighbour will no longer be laying, and dumping eggs, and because the neighbours’ own aggressive behaviour may fortuitously keep other birds away from both their nests (Møller 1989b). Because the sex ratio in groups tends to be biased towards males, females usually find mates soon after arriving in spring. Female visitors to nests are therefore likely to be breeding or to have recently attempted to breed themselves. Crook & Shields

14639.qxd

24/1/06

3:53 pm

Page 97

Breeding strategies

97

(1987) found that 39% of female visits occurred within three days of a nest failure and suggested that the females may still be showing parental care or looking for alternative nest sites. Sometimes, females may visit nests while still unattached. Crook & Shields (1987) noted one unmated female taking over another female’s mate and nest, throwing out the eggs, and Medvin et al. (1987) recorded two females visiting nests and eventually mating with the male of the pair, one when his mate died and one polygynously. Although it is not known if these latter two females were unattached or had lost their mates, the fact that they were visiting the nests at the beginning of May suggests the former.

PAIR BONDS After rearing one brood, pairs often stay together to rear a second that season and reunite the following year if both survive. However, the mortality rate is such that many birds are widowed between years. In Scotland, 15% of 150 pairs were together for two years and only two pairs for three years (Thompson 1992). In one German study of 267 pairs, only 17 pairs were together for two years, two pairs for three years and one pair for four years (Brombach 2004). In Denmark, Anders Møller (pers. comm.) recorded one pair breeding together for five years. Both males and females sometimes leave their mates and nest sites to try to breed elsewhere. This can happen both within and between breeding seasons and is often, but not always, the result of a pair failing to breed together successfully. Sometimes, pairs divorce at an early stage after being together and copulating for only a few days (Møller 1985). In Shields’ study (Shields 1984a), 42% of pairs that bred successfully in one year stayed together the next, but all those that failed went on to split up. In these cases it was the females, not the males, who were more likely to change nests after a failure than after breeding successfully. Divorce was less likely within a breeding season, with 78% remaining faithful to their mates for a subsequent brood; and failed breeders were only marginally more likely to leave their mates than successful ones. There was no evidence that pairs tended to divorce after a failed breeding attempt in other populations in Scotland (Thompson 1992), Italy (Saino et al. 2003f ) or New York State (R.J. Safran, pers. comm.). Saino et al. (2003f ) also found that divorcing a mate and pairing with another one did not significantly improve a bird’s breeding success, although birds tended to breed later after a divorce.

14639.qxd

24/1/06

3:53 pm

Page 98

CHAPTER 6

Nest sites and nests . . . the twittering swallow hangs its nest from the rafters. Virgil, c. 30 B C

Barn Swallows breed in many different habitats, but are particularly closely associated with farmland, which provides suitable sites both for feeding and for nesting. Although once cave-dwellers, Barn Swallows nowadays nearly always opt for human artefacts such as buildings as nest sites, and farmyard barns and cattle stalls are favourite locations. This close association with people is seen in the names of Barn Swallows in various countries – such as Hirondelle de Cheminée in France and Rauchschwalbe in Germany. In Britain in the nineteenth century Barn Swallows were also often called Chimney Swallows. The name refers to their habit of nesting on ledges in chimney stacks, a now scarce site (Holloway 1996). In many Asian countries they are known as House Swallows, as they nest in shops and other occupied buildings; they are considered a good luck symbol and people encourage them to nest by putting up ledges for them. In contrast, Americans have long called the

14639.qxd

24/1/06

3:53 pm

Page 99

Nest sites and nests

99

species the Barn Swallow because, at least when European settlers first came, it became associated with unoccupied farm buildings. According to Bent (1942): ‘In the rural districts of old New England, the old-fashioned barn, with its wide-open doors and its lofty haymow, seems to be the most common and most characteristic nesting place’.

BREEDING HABITAT Good breeding habitat needs abundant feeding sites such as waterbodies and trees or hedges, which provide good sources of insects during bad weather (Chapter 2). Lakes, ponds and rivers are particularly important early and late in the breeding season during cold spells at high latitudes, when they are the main source of insect prey. An analysis of the British Breeding Bird Survey data, at the resolution of 1-km grid cells, in relation to habitat type found more Barn Swallows in areas with a large area of water or a high proportion of farmland and fewer in those with heathland and bog (Evans 2001). In farmland, Barn Swallows clearly selected grazed grassland rather than ungrazed grassland or arable. The amount of scrub had a slightly positive effect on numbers of Barn Swallows, whereas woodland was generally not preferred habitat, although woodland edge can provide good feeding sites. In Scandinavia, Söderström & Pärt (2000) similarly found few Barn Swallows in heavily forested areas; and North American surveys have also recorded few or no nests in either extensively forested areas or dry areas with few trees (e.g. Brewer et al. 1991; Palmer-Bell 1996; Nicholson 1997; Kingery 1998). Nevertheless, Barn Swallows will breed in a wide variety of habitats, including lake or river shorelines, parkland, woodland clearings, wetlands and sand dunes; some pairs even nest in the tundra where humans have put up cabins or other buildings (Peck & James 1987). Indeed, few types of habitat are totally unsuitable. Although densely populated built-up areas are rarely used in Europe, Barn Swallows will nest along busy streets in towns and cities in Asia and North Africa (e.g. Mizuta 1963). In North America, too, Barn Swallows sometimes nest on bridges along watercourses in cities such as Denver (Kingery 1998). A combination of air pollution and improved sanitation, making its insect prey scarce, may explain the Barn Swallow’s general absence from Western cities. For example, only one pair has nested in inner London (in Regent’s Park) since 1908 (Oliver 1997). Northern House Martins did return to breed in London after the 1956 Clean Air Act, but this species feeds on smaller prey and at higher altitudes; the Barn Swallow’s prey may not have recovered to the same extent. A decline in numbers of Barn Swallows in cities in Romania may be the result of air pollution (Munteanu 1998). Barn Swallows are mainly a lowland species. In Europe, relatively few pairs nest above 1,000 m; breeding is regular up to about 1,200–1,300 m in some areas, such as the Austrian and Swiss Alps, occasionally up to 1,400 m in the Krkonose Mountains in the Czech Republic, with a few Swiss records as high as 1,920 m

14639.qxd

24/1/06

3:53 pm

Page 100

100

The Barn Swallow

(Møller & Vansteenwegen 1997; Schmid et al. 1998; Isenmann 1999; Kren 2000). In Switzerland, Barn Swallows occur in fewer villages at higher altitudes (Schifferli et al. 1984). Further to the north-west in Scotland, the altitude limit is much lower; breeding pairs are relatively scarce above 400 m and especially above 600 m (Buckland et al. 1990; Murray et al. 1998). In Asia and North America, Barn Swallows also nest mainly up to 1,000 m, but sometimes up to c. 3,000 m, for example in the Caucasus and Colorado (Cramp 1988; Kingery 1998). The fact that some habitats such as tundra and moorland have few Barn Swallows except where people have put up buildings suggests that it is sometimes the availability of nest sites, rather than just the climate and availability of food, that determines the suitability of locations for breeding. Murray et al. (1998) suggested that the lack of nest sites was the main reason for the scarcity of Barn Swallows breeding in upland areas of south-east Scotland. However, all three factors are likely to be important and may interact. In Scotland, the habitat in upland areas is mainly moorland and forest with few human settlements. The climate is also cool and wet and the soils are poor. Insects are therefore less abundant, and the weather is likely to be poor in spring. This makes it difficult for females to lay eggs and incubate them early in the year. In north-east Scotland, Barn Swallows in upland areas are associated with plantations which may provide more food and shelter than moorland (Buckland et al. 1990). In contrast, in the Alps, sunny valleys, traditional small farms with cows and large areas of pasture may allow Barn Swallows to breed at higher altitudes by providing sheltered nest sites and abundant insects (Isenmann 1999). Spring temperatures at such sites are important and need to be high enough to support a good food supply. In Switzerland, villages with cool local climates are less likely to be used by Barn Swallows than those in milder sites, especially if they also have a lot of rain (Schifferli et al. 1984).

NEST SITES Natural nest sites seem to be rarely used by Barn Swallows nowadays; the majority nest in or on human-made structures, although the inaccessibility of some natural sites may mean that their use is under-reported. Natural sites are, and were in historical times, predominantly in caves. Crevices and holes in cliffs, rock outcroppings, river banks, sinkholes and, less often, tree limbs and hollow trees were also used (e.g. Cramp 1988; Nikolaev 1998; Brown & Brown 1999a). Across the breeding range, few regular natural sites are known. In Britain, however, there is evidence of Barn Swallows nesting in caves at Cresswell Crags, Derbyshire, 15,000 years ago and small numbers still nested there in the 1980s and 1990s, although not in the past few years (Derbyshire Bird Reports; R. Frost & R. Key, pers. comm.). Numerous artificial sites are used throughout the breeding range, including the insides of derelict buildings, stables, barns, sheds and garages, mine shafts, wells, under bridges and jetties and in culverts. In Europe and Asia, Barn Swallows are

14639.qxd

24/1/06

3:53 pm

Nest sites and nests

Page 101

101

associated particularly with indoor sites, such as farm buildings, houses or shops. Studies in northern and central Europe have recorded relatively few nests built out of doors, under eaves or in balconies, for example (e.g. Denmark 5%, Møller 1983; Austria 2%, Landmann & Landmann 1978; Scotland and Poland, under 1%, Thompson 1992; Kartanas 2001). This may be more common in warmer areas, however: in northern Italy, for example, 22% of pairs used outdoor nests (R. Ambrosini, unpubl. data). In some parts of Asia, Barn Swallows regularly nest under eaves of shops and houses (e.g. in Japan, Mizuta 1963). North American Barn Swallows also often nest in exposed places such as under the eaves of buildings, under wharves and, increasingly, under bridges and in culverts. In studies in Ontario and Kansas 15% and 8%, respectively, of nest sites were under bridges and in culverts (Anthony & Ely 1976; Peck & James 1987). This may be partly because of the abundance of bridges and culverts, especially in areas where buildings are scarce, such as along highways, but also because North American Barn Swallows have had less time to develop a close association with people than other subspecies have. In addition, in southern states such as Florida, nest sites over water may have a cooler, more favourable microclimate than indoor ones (Stevenson 1978). In Argentina, too, where Barn Swallows have recently started breeding, they extensively use bridges and culverts (Petracci & Delhey 2004). Barn Swallows have probably been nesting on human artefacts for thousands of years. They were well known to the ancient Egyptians, who considered them a minor deity and often mummified them, and to the Romans and other ancient civilisations around the Mediterranean. Barn Swallows in North America are known to have nested on Native American habitations at least in the early 1800s, when natural sites were still commonly used (Brown & Brown 1999a). Colonisation of areas by Europeans, however, has had a big impact on where the birds nest. There were many reports of natural sites being used in North America in the second half of the nineteenth and in the early twentieth centuries, for example, but such reports are now relatively rare compared with the many artificial sites used (e.g. less than 1% of nests in Canada are reported to be on natural sites: Erskine 1979; Brown & Brown 1999a). Buildings, bridges and other human-made constructions have provided many new sites, especially in inland areas with few natural ones. This, together with the provision of new feeding opportunities where forest has been cleared and livestock introduced, has allowed populations of Barn Swallows to expand their breeding ranges and increase in numbers (Chapter 11). Where people have immigrated into new areas, Barn Swallows have followed. Russian immigrants into the Amur region in the seventeenth century, for example, provided sites where Barn Swallows from different areas met (Smirensky & Mishchenko 1981). In North America too, Barn Swallows followed newly built railways, nesting in the towns as they sprang up. The expansion of Barn Swallow populations into northern Alberta in the 1960s has been attributed to new farming and oil-prospecting ventures, and their expansion southwards in Mississippi, Alabama and Louisiana, also in the 1960s, to increased construction of roads and concrete bridges (Jackson & Burchfield 1975; Erskine

14639.qxd

24/1/06

3:53 pm

Page 102

102

The Barn Swallow

1979). Jackson & Burchfield suggested that older wooden bridges were unsuitable as nest sites because they were often painted with creosote, which may give off noxious fumes, had cracks through which dust could drop, and were more accessible to climbing predators such as snakes.

NEST SITE REQUIREMENTS Substrates and building materials The substrate for nests needs to be rough enough to provide sites of attachment. Beams are ideal but cracks, corners and projections from a wall are all suitable if a horizontal support is not available. Objects attached to a wall or hanging from a roof or beam also provide support: these have included wasps’ nests, old birds’ nests (conspecific ones or those of other species including Cliff Swallows, Black Redstarts, European Robins, Eurasian Blackbirds, Song Thrushes, Eastern Phoebes and American Robins), picture frames, hats, pieces of cloth, lampshades and brackets, electric wires, masonry bolts, nails, chains, gear wheels and pulleys, a sunflower seedhead nailed to a beam and the corpse of an owl! Beams, however, are often the main support used. For example, of 192 nests in Scotland, 41% were on beams, 38% in a roof apex, 6% on walls and 15% on other sites (McGinn & Clark 1978) and in British Columbia, 46% of 2,537 nests were on beams or rafters, with 18% under eaves, 11% on projections or ledges, 9% on walls and 5% over light fixtures (Brown & Brown 1999a). In contrast, in Stavropol, Russia, a third of nests were attached to walls, and a quarter each on beams and in the angles between walls (Akopova et al. 2000). Nests supported from below on permanent fixtures such as beams are likely to last longer than unsupported ones. Møller (1983) found that only 2% of supported nests, but 13% of unsupported ones, fell down. Wood is rough enough to provide a ready attachment site, whereas cement, metal and plastic are poorer substrates, unless there is a projection from the surface such as a nail. Jackson & Burchfield (1975), studying nests on bridges, found 78 nests were built onto cracks, wasps’ nests and masonry bolts and only 20 on the relatively smooth surface of the concrete. In metal culverts, Barn Swallows use bolts for support (Brown & Brown 1999a). Barn Swallows are very tolerant of their nests being disturbed or moved. They can even nest successfully on moving objects such as oil pumps, trains and boats, including a barge that moved between Rotterdam and the Ecofisk oilfield in the North Atlantic, and ferries in Denmark (e.g. Swarth 1935; Buckland et al. 1990; Brown & Brown 1999a; A.P. Møller, pers. comm.). In such circumstances, the parents either forage in sight of the nest if it is moving slowly enough, or await its return. It is possible to move nests to new sites provided it is done slowly. For example, in an attempt to found a population at a new site, Winkler & McCarty (1990) successfully moved two nests 3.5 km in 27 hours and 13 hours of daylight, respectively. In less extreme circumstances, if a nest falls down, the chicks can be put in a box close

14639.qxd

24/1/06

3:53 pm

Nest sites and nests

Page 103

103

by, out of the reach of predators, and the parents will return to feed them. In such circumstances, the parents may at first go to the original nest location, but they soon direct their attention to the new site, even if the latter is not fixed. As well as a means of support, a nearby source of building materials, both mud for the nest itself and dry grass and feathers for the lining, is also necessary. These materials are usually easily obtained, but can be scarce, for example in dry weather. Urban areas may also be poor sources of suitable material: this was the reason for 5% of nests failing in a study in Hiroshima (Suzuki 1998).

Perches and access Perches near the nest but out of the reach of predators are needed as song and display posts and for other activities such as preening, sunbathing and foraging sorties. For example, Jackson & Burchfield (1975) found that bridges with adjacent utility wires were preferred to those without. Nest sites must also provide a clear flight path for rapid and safe access and egress. Barn Swallows do not need open sites or large entrances to enclosed sites, though; they can use surprisingly small holes, and 5×7 cm is enough of an opening to gain access to a building. One pair in Minneapolis, USA, learned to open an automatic door to get to their nest (WABC-TV 2004). Nests are usually built close to the point of access and if there are several nests in one building there may be several such points (e.g. Møller 1983; Thompson 1992). Adult Barn Swallows are generally faithful to their nest sites between years (Chapter 10), but changes in use of buildings and in access could affect their choice of sites.

Safety and shelter An important requirement for suitable nest sites is that they be safe from predators and bad weather. To avoid ground predators, nests are usually built high up in buildings, on average about 2–4 m above ground level. In a Scottish study, for example, 41% of 189 nests were at 3–4.5 m, 38% at 2–3 m, 16% over 4.5 m and only 5% less than 2 m above the ground, with an average of 3.3 m (McGinn & Clark 1978). Nests are also usually built a few centimetres from an overhang or roof, and away from places giving climbing or avian predators access. In natural cave sites, nests are also built on ledges close to the roof (Speich et al. 1986; Brown & Brown 1999a). Nests are usually built in sites protected from the wind and rain, either in buildings or under eaves, or, if under bridges, well away from the edge. Thus, Jackson & Burchfield (1975) reported that pairs preferred short, wide bridges facing north–south which may have sheltered them from the prevailing winds. Lohoefener (1980) found that Barn Swallows nesting in culverts preferred those longer than 0.9 m, perhaps because they provided better shelter, and in caves the nests are built about 3–7 m from the opening (Brown & Brown 1999a). Sites close to a roof in a building are usually warmer and the temperature is less variable than in exposed sites (e.g. Møller 1983 recorded temperatures of 17–28.9°C inside nest sites versus

14639.qxd

24/1/06

3:53 pm

104

Page 104

The Barn Swallow

3–30°C outside), which may help to keep the eggs and young chicks warm. However, overheating can be a problem in such sites (Chapter 9). Outside sites are inherently more exposed to predators and the weather and may often be avoided except in mild or warm climates where shelter is less necessary or where inside sites may get too hot (Stevenson 1978; Murano et al. 2000). In some places, however, such as along highways in North America, outside sites such as bridges may be the only available places to nest. Nest sites are also often in dark places: Møller (1983) recorded 83% of sites with illumination below 300 lux and Landmann & Landmann (1978) recorded 89% below 200 lux. The low light levels may provide additional protection from visually hunting predators.

Artificial nests Barn Swallows will sometimes use artificial nest supports and nests. Pieces of wood, up to about 15 cm wide, nailed up in appropriate places, such as a dark corner of an outbuilding, can serve as ledges for Barn Swallows to build nests, and artificial nest cups are now available commercially. However, the success of artificial nests is variable; in Denmark, Barn Swallows were not attracted to them (A.P. Møller, pers. comm.), whereas in Maryland, USA, they seemed to prefer artificial nests to natural ones (van Vleck 2004). Artificial nests should be put up in sites protected from the weather, including high summer temperatures, and with permanent access, preferably two to three metres high and with a clearance of four centimetres from the ceiling; it is also helpful to provide a source of wet mud for nest-building and crushed eggshells for grit, and to clean out the nest once a brood has fledged to remove parasites (van Vleck 2004).

Habitat quality A variety of artificial constructions meet the requirements for suitable breeding sites, but farm buildings with livestock are particularly popular, at least in Europe (e.g. Landmann & Landmann 1978; Møller 1983, 2001b; Ambrosini et al. 2002a, b). In Italy, for example, Barn Swallows bred on 91% of farms with livestock, but on only 44% of farms without; and there were more Barn Swallows on farms with traditional stabling than on those with no stabling or with modern cattle barns (Ambrosini et al. 2002a). Of all livestock, Barn Swallows seem to associate most with cattle. Møller (1983) and Loske (1994) found that cowsheds were preferred sites, with pig sheds being used more as spill-over sites when the Barn Swallow population was large. Over 30 years, 84% of 2,194 pairs in Denmark bred on dairy farms (Møller 2001b). Surveys in the Netherlands, Poland and the Flanders region also noted that buildings housing cattle and pigs were important breeding sites (Windig & Florus 1997; Kartanas 2001; van den Brink 2003). Horse stables are popular nest sites as well, when available; other structures for housing livestock such as poultry and rabbits are also used but to a lesser extent. However, Barn Swallows readily nest in buildings and on farms with few or no animals. In Scotland, for example,

14639.qxd

24/1/06

3:53 pm

Nest sites and nests

Page 105

105

they frequently used traditional stone-walled barns and less than 1% of nests were in buildings where livestock were kept (Thompson 1992). Some studies have recorded better breeding success in buildings with livestock, but this may be at least partly because high-quality sites may attract older or betterquality birds, which have larger broods anyway. In Germany, for example, pairs breeding in cattle sheds were both older and had better annual breeding success (7.3 fledglings per pair) than those in pig sheds (6.3 fledglings) or other buildings (5.5 fledglings; Loske 1994). A potential benefit of nesting in livestock stalls is that animals are likely to keep the stall relatively warm and at a fairly constant temperature even when the outside temperature is cold. This may help the energy budget of incubating birds and young chicks, allowing the females to be away from the nests for longer without the eggs or chicks chilling (Chapter 7). How important this is is not clear, however. The type of building may itself affect the birds’ energy balance and breeding success, regardless of the presence of animals: stone buildings, for example, may provide better protection from extremes of weather than wooden structures. Some types of building may have other advantages or disadvantages. A survey of breeding success of Barn Swallows in the Netherlands in 1992–98 found that, on average, they produced about 0.5 fewer fledglings per clutch in modern free-stall barns than in other types of building, in part because of easier access by predators and displacement by House Sparrows (van den Brink 2003). Breeding sites must also have access to good feeding sites, and farms with livestock are ideal in this respect, too (Møller 2001b; Chapter 2). The presence of animals itself is beneficial. Animals kept inside or cattle moving between field and yard for milking, and the resulting manure heaps, attract insects around the farmyard, providing food for the Barn Swallows close to the nest (Loske 1994). In addition, livestock grazing outside provide good feeding sites for Barn Swallows: besides attracting flies to themselves and their dung, they also rout insects from the vegetation as they walk. Livestock also have long-term effects on invertebrate populations by grazing and producing dung. However, these effects vary with the type of livestock, their stocking density and management. Sheep graze very close to the ground, resulting in a short sward and a smaller, less diverse invertebrate community than in the longer sward left by grazing cattle; cattle also leave larger piles of dung that is attractive to insects (e.g. Vickery et al. 2001). Cattle thus probably increase the abundance of insects in a field in the long term, although the short-term effects of livestock and their dung are probably more important for aerial insects (Evans 2001). Fields kept for livestock provide more insects than do cereal or other crops, and are preferred by foraging Barn Swallows (Evans et al. 2003a). In addition, Evans (2001) recorded more insects and more types of flies within 10 m of cattle than 20 m or more away, particularly those associated with dung. Møller (2001b) found that insects were twice as abundant on farms when they had dairy cattle than when dairying was abandoned. In Britain, Barn Swallows are most abundant in areas with cattle-grazed pasture, compared with sheep-grazed and ungrazed pasture and arable land (Robinson et al. 2003; Figure 6.1).

14639.qxd

24/1/06

106

3:53 pm

Page 106

The Barn Swallow

Figure 6.1. More Barn Swallows are recorded on cattle-grazed pasture than on sheep-grazed or ungrazed pasture and arable fields. Bars show mean number of individuals (and 95% confidence limits) on 200-m transects on Breeding Bird Survey plots. From Robinson et al. 2003.

Although, in general, livestock are beneficial for foraging Barn Swallows, Evans (2001) found that the birds appeared to avoid areas where cattle were stocked at densities higher than 20 livestock units per hectare; he suggested that in this situation intensive grazing and greater use of chemicals may reduce the number of insects, and that the cattle themselves might be obstacles to flying Barn Swallows, interfering with their foraging. Livestock may be particularly important in areas with cool climates. Thus, Møller (2001b) found that Danish Barn Swallow numbers declined when dairy farms went out of business, whereas in Italy the effect on Barn Swallows of the loss of farms with cattle appeared 7–8 years later (Ambrosini et al. 2002a,b). In northern latitudes, cool, wet weather may make Barn Swallows more dependent on the insects associated with livestock or on the warmth of their stalls, hence heightening the effect of any loss of livestock (Ambrosini et al. 2002b). In Hokkaido, at the northern edge of the range in Japan, cowsheds seem to allow Barn Swallows to breed in the cool north and east, where few nest under eaves, in contrast to those in the south and west, where eaves are common nest sites (Murano et al. 2000). At any latitude, however, the presence of livestock is likely to be beneficial during long periods of bad weather. In North America, Barn Swallows are likely to be less dependent on livestock, because males help to incubate and so the eggs are less exposed to low temperatures. Besides livestock, other features of the habitat such as waterbodies and shelterbelts provide good feeding sites. The Barn Swallows’ preference for feeding in such sites was described in Chapter 2, and I return to this subject in Chapter 11, when considering the causes of recent population changes.

14639.qxd

24/1/06

3:53 pm

Page 107

Nest sites and nests

107

NEST SIZE AND STRUCTURE The nest is an open cup made of mud, mixed with variable amounts of bulky material such as dry grass, straw and horsehair. It may contain 750–1,400 pellets of mud (Glutz von Blotzheim & Bauer 1985). When the usual materials are scarce, Barn Swallows will substitute others, including dung, pine needles, cotton, seaweed, algae and sphagnum moss (e.g. Bent 1942; Duffin 1973; Landmann & Landmann 1978; Nikolaev 1998), and occasionally the nest consists largely of straw or grass stalks. Sometimes distinct layers are visible where different mud has been used or is interspersed with grass (Brown & Brown 1999a). In the USA, Kilgore & Knudsen (1977) noted that Barn Swallow nests had a relatively low sand and high silt and clay content. Since sand reduces the compressive and tensile breaking strengths of adobe, Kilgore & Knudsen (1977) suggested that the high silt and clay content of the Barn Swallow’s nest helps to make it stronger. In addition, the organic material in the nest helps to bind the pieces of mud together and may increase the tensile strength. The newly built nest is usually about 20 cm wide and 10 cm high. In one study, for example, nests were 12–26 cm in diameter (average 18 cm) and 5–18 cm high (average 10 cm) with a nest cup of 8–17 cm in diameter (average 11 cm) and 4–8 cm deep (average 6 cm); they weighed 255 g on average, including 10 g of lining material (Akopova et al. 2000). Six nests at a natural rock site measured 9–11 × 13–20 cm externally with a nest height of 8–15 cm and 7–11 × 9–12 cm internally with a nest cup depth of 4–9 cm (Nikolaev 1998). The shape varies depending on where the nest is built: it is usually a fairly flat-bottomed half-sphere on a horizontal support or a deeper quarter-sphere on a vertical one, but sometimes a corner site, or a crevice in a rock in natural sites, needs no mud or only a wall built across it. Occasionally, when abandoned nests of other species are used, some mud may just be added to the rim (Glutz von Blotzheim & Bauer 1985). The nest is lined first with dry grass and then with soft hair and feathers. Occasionally, other material such as wool, cotton and paper becomes incorporated into the lining. Feathers may continue to be added during egg-laying and incubation. White chicken feathers are the most popular type of feather; the use of white feathers, together with the pale eggs, may help the parents find the nest in dark sites (Møller 1983). Feathers insulate the nest and so help to reduce the rate at which the eggs cool when the female is not sitting on them and to increase the rate at which they warm up when she returns (Møller 1991c). The feathers are gradually removed as the chicks grow, however, probably because well-grown chicks are more at risk of overheating if the nest is too warm. Møller (1987b, 1991c) counted on average up to 33.5 feathers per nest and a reduction of 70% during the chick-rearing period; there was no relation between numbers of feathers and nest size.

14639.qxd

24/1/06

3:53 pm

Page 108

108

The Barn Swallow

NEST-BUILDING AND RE-USE Building a nest from scratch generally takes 5–12 days, longer if bad weather curtails the time available for this activity. Dry weather when wet mud is unavailable also delays proceedings. Nests can be built in as little as three days or as long as 17 days (e.g. Thompson 1992; Brown & Brown 1999a). Nest-building may start within a few days of the birds arriving, but pairs that arrive early may have more time for building and take longer over it while waiting for conditions to be favourable for laying, whereas late pairs may build more intensively and quickly. The lining usually takes a few days to add, with feathers being brought to the nest a few days before the female is ready to start laying. Thompson (1992) noted that grass was added five days, and feathers three days, before laying started and that the state of the lining could be used to predict laying to within a day or two. Most building work is done in the mornings; this probably serves to allow the mud to dry before nightfall and to allow the birds to feed in the warmest part of the day and before they go to roost. The birds need to allow the recently applied mud to dry, because too much wet mud would distort the nest under its own weight before it dried out (Hansell 2000). In Scotland, Barn Swallows each spent about two hours a day working on the nest, with 8.5 trips per hour on average and 20–25 trips per hour during the most intense period (Turner 1980). Møller (1994a) reported an average of 30 trips per hour per nest (range 5–42). As well as time of day, the weather and food supply also affect the time devoted to building, as bad weather may force Barn Swallows to spend their time feeding. In contrast, on good days, males will spend more time perching and singing (Turner 1980). Both males and females are involved in nest-building, but the relative contribution of each sex depends on the quality of the male as a breeding partner. Although males on average do about a quarter of the work, their contribution to nest-building ranges from 0 to 68% (Møller 1994a). In Europe, males with long tails (that is, those most attractive to females) do relatively little nest-building and so their partners have to do most of it (Møller 1994a; Soler et al. 1998). Shorter-tailed males, on the other hand, contribute more to building the nests. Females mated to longer-tailed males build nests with a large volume, to accommodate a large clutch. However, they do not use more mud in the process than do pairs with short-tailed males, so they end up with large nests with thinner walls. The thickness of the wall does not seem to affect the success of the brood (Soler et al. 1998). Nests containing a lot of material are thus built by pairs in which the male contributes substantially to the building. There are cases where a male and a female have each made a nest but only the female’s was eventually used (Radermacher 1989; A.P. Møller, pers. comm.). Barn Swallows collect mud from any source, be it a stream’s edge or the hoofprint of a cow. In Scotland, the average round–trip time to collect mud, from sites 10–30 m away, and to add it to the nest was two minutes (Turner 1980). A nest can require a thousand or more trips to collect mud (e.g. Purchon 1948; von Vietinghoff-Riesch 1955). Wood (1937) estimated that a pair of Barn Swallows

14639.qxd

24/1/06

3:53 pm

Nest sites and nests

Page 109

109

had flown 137 miles (220 km), making 1,359 trips or 100 per day per bird, to build their nest. The first stage of nest-building is the construction of a ledge or base on which the Barn Swallows can perch. They then build the walls upwards and outwards. Barn Swallows collect a billful of mud at a time, usually spending only a few seconds on the ground. At the nest the mud is manipulated into position with the tongue and bill and the bird vibrates its head up and down to tamp down the mud. This probably disperses the mud into any air spaces, thus preventing cracks forming (Hansell 2000). Hansell also suggested that liquid mud carried on the top of the bill might be used to bridge the gap between the mud pellet and the nest, again avoiding the development of cracks, but it is not clear how often Barn Swallows do this. Alternatively, mud on the top of the bill may have got there just by accident (Snape 2002). The bird sometimes wipes its bill afterwards on, for example, a feather (Snape 2002). Barn Swallow nests are sturdy structures and can last for several years; von Vietinghoff-Riesch (1955) reported nests being used for up to 48 years, but more usually 12–15 years and Radermacher (1989) reported nests being used on and off for up to 24 years. One nest in Radermacher’s study was used for 11 broods and another for ten. Brown & Brown (1999a) reported nests at least 17 years old that had been built up with new mud each year to more than 70 cm high. So birds returning to their breeding sites usually have the option of re-using an old nest rather than building a new one; similarly, after the first brood has fledged, the parents can re-use the same or another nest. In Scotland, for example, old nests were used for 76% of first broods and 21% of second broods; 68% of double-brooded pairs who used an old nest for the first brood also used an old nest for the second (Thompson 1992). Similarly, Loske (1994) recorded 85% of pairs using the same nest for both the first and the second broods. Shields (1984a) found that 53% of pairs re-used a nest within a breeding season and 44% between seasons. Parent birds potentially save time by not building anew, particularly if the weather is not favourable for such activity. An old nest often needs only a little extra mud to bolster any crumbling edges; and this can be collected in just a few days. A new feather lining is also usually added. Both mud and feathers may be added after the first brood, ready for the second if a nest is re-used within a season (e.g. Samuel 1971b). Shields et al. (1988) found that Barn Swallows repairing old nests needed 10–50% of the time taken to build new ones (an average of 4.8 versus 11 days). Whether this time saving is important may depend on the time of season. Early in the season, when laying starts may depend more on the weather and food supply than on whether the pair has to wait while building a new nest. In Barclay’s study (Barclay 1988), for example, in May eggs were laid on average 7–9 days after work on the nest had started for both new and old nests; later in the season, however, pairs using old nests laid after three days, significantly sooner than pairs making new nests, which still took a week. Radermacher (1970) also recorded repairs to old nests starting on average eight days (range 0–15) before the first eggs were laid, similar to the 5–11 days taken to build a new one. Thompson (1992) found that pairs building a

14639.qxd

24/1/06

110

3:53 pm

Page 110

The Barn Swallow

new nest started laying about four days later than those using old ones, but repairing a nest still took six days on average (range 3–16) compared to nine days to build anew (range 6–17). Although the time saving may be a small part of the whole season, and pairs may have enough time to build a new nest and still rear two broods, starting each brood as early as possible may help improve the long-term survival of the chicks and thus their chances of recruiting into the population (Thompson 1992; Møller 1994a). Very early breeders are also more likely to have a second brood and may also have time for a third one. Barn Swallows that re-use a nest also make fewer trips to collect mud, so both save energy and reduce the risk of being caught by predators while on the ground. In addition, existing nests are already likely to be sited in the best places, safe from the weather and from predators. Birds that re-use nests that have been successful in the past will be assured of a good site, whereas birds building in a new site may find problems with that site later in the season. Safran (2004) found that pairs with old nests produced 25% more fledglings than those laying at the same time in new nests at the start of the season, suggesting benefits of re-using a nest other than just a time saving. However, not all studies have found an increase in breeding success associated with re-using nests (Barclay 1988; Shields et al. 1988). Nests do not last forever; changing temperatures and moisture content eventually break up some nests, while others are blown down by wind, or destroyed or pulled down by predators or humans and some are taken over as nests by other species (Chapter 9). Because unstable nests might fall and crush eggs or chicks, it could sometimes be better to build a new nest than risk using an old one. Many unstable nests may fall during the winter before the Barn Swallows return, but nest falls also occur in the breeding season (e.g. Shields & Crook 1987). However, Thompson (1992) recorded few nest falls and found that even new nests could fall down, while Safran (2005) found that new nests were more likely than old ones to fall down during a breeding season, so this may not always be an important disadvantage of old nests. Another reason for not using old nests is that they may harbour parasites which can harm the chicks (Barclay 1988; Shields et al. 1988; Safran 2005; Chapter 8). In an experiment in which he changed the numbers of mites in old nests, Møller (1990a) found that Barn Swallows will avoid infested nests: he sprayed some nests with a pyrethrin solution to kill the mites, and added mites to other nests. While 65% of nests without mites were re-used, only 25% of nests with ten mites, and no nests with 100 mites, were re-used. In addition, naturally infested first-clutch nests were often not used for second clutches (Figure 6.2). Since many parasites will die if the nest is left empty for a year, Barn Swallows may be able to avoid nests with parasites by using alternative old nests available in their territory. Barclay (1988), for example, found that pairs selected nests without mites for their first brood. Building a new nest may therefore sometimes be the best option, if the old nests have lots of parasites, for example, or it may be as good an option as re-using an old one or it may just be the only course open to the birds. Barn Swallows arriving late in the season may, for example, find that the most suitable old nests have been taken

14639.qxd

24/1/06

3:53 pm

Nest sites and nests

Page 111

111

Figure 6.2. Barn Swallows are less likely to build a new nest for their second clutch if their first-clutch nest had no or few mites. After Møller 1990a.

or are too close to another pair at a nearby nest, and these birds may then have to build a new one. Indeed, first-year birds, which arrive after older birds, are more likely to build new nests (Shields et al. 1988). In Loske’s study (Loske 1994), 14% of pairs built a new nest and almost all of these pairs included at least one first-year bird. It is not clear, however, how free individuals are to choose between re-using a nest and building a new one; some aggressive Barn Swallows may actively prevent others from using a nest nearby and force them to build elsewhere. In contrast, dry weather may force pairs to re-use a nest, if wet mud is unavailable to build a new one.

14639.qxd

24/1/06

3:53 pm

Page 112

CHAPTER 7

Eggs and incubation And now, suddenly, into a blanch-tree stillness A silence of celandines, A fringing and stupor of frost She bursts, weightless– To anchor On eggs frail as frost. Ted Hughes, 1981

Egg-laying is a critical stage in the Barn Swallow’s life cycle. Winter has barely gone and the weather can still turn severe when Barn Swallows return to the breeding grounds. If feeding conditions are not good, laying can be delayed, with consequences for the clutch size, the number of broods that the birds have time to rear, and even for recruitment of offspring into the breeding population in the following year. From the numerous studies that have recorded details of the Barn Swallow’s breeding biology in a variety of weather conditions and habitats, the importance of the

14639.qxd

24/1/06

3:53 pm

Page 113

Eggs and incubation

113

food supply is clear. However, there are still aspects that have yet to be explored, such as the reasons for differences in incubation behaviour between the subspecies.

BREEDING SEASON The breeding season varies across the range of the Barn Swallow (Glutz von Blotzheim & Bauer 1985; Cramp 1988; Brown & Brown 1999a). Egg-laying usually starts in February or March in southern populations and late May to early June in the northernmost ones. In Britain, the laying period extends from late April to September, but usually starts in early May in the south and a week later in the north, and usually continues until mid-August. Laying peaks in mid-May to mid-June and in July for first and second clutches, respectively. First broods typically fledge in June and second broods in late July or August. Breeding usually finishes before the weather deteriorates, with most broods fledging by early to mid September. Some very late second broods and third broods, however, have fledged in October. Egg-laying occurs over an extended period, both because some females have more than one brood and because they arrive on the breeding grounds at different times. Those starting late generally have only a single brood whereas those starting early will have two or three. First clutches can be laid over several weeks, although the degree of synchrony in laying between females is variable. Snapp (1973), for example, recorded spreads of 5–30 days in different groups over two years. Second broods are more synchronous. Groups may become more synchronous, however, if bad weather delays breeding by the earlier birds (Snapp 1973). The first laying dates within a population can vary considerably between years, as do dates of arrival on the breeding grounds (Chapter 10). In Scotland, for example, I recorded a late first laying date of 17 May and Thompson (1992) recorded an early one of 4 May. In part this variation is linked to how good the feeding conditions are on the Barn Swallows’ wintering grounds and migration route, because these partly determine when they first arrive on the breeding grounds and hence how early they can breed (Chapter 10). Generally, but not always, laying dates are closely tied to arrival dates (e.g. Ninni et al. 2004; Saino et al. 2004c). Individuals usually arrive a week or more before starting to lay, an average of 16 days in Møller’s study (Møller 1994a), for example. However, there is sometimes a delay of several weeks (e.g. Anthony & Ely 1976; Ribault 1982), and Spanish Barn Swallows generally arrive three weeks to more than two months before breeding starts (Møller et al. 2003). The number of broods that can be reared and the probability of chicks surviving to breed themselves decrease with time during the breeding season (Chapter 9), so one would expect females to start laying as soon as possible in the spring, provided food is sufficiently abundant (Perrins 1970; Bryant 1975). Flying insects rapidly proliferate during the spring as the weather improves, and Barn Swallows may thus wait until insect abundance reaches a certain level before laying. A good and stable

14639.qxd

24/1/06

114

3:53 pm

Page 114

The Barn Swallow

food supply is particularly important by the time Barn Swallows start incubating, because the females’ foraging time is constrained by the need to incubate the eggs and to avoid leaving them for long periods. Environmental conditions on the breeding grounds clearly affect when laying starts. In Scotland, the timing of breeding depends on the abundance of insects: when food is plentiful, breeding both starts earlier and ends later, and brood sizes are larger (T. Benton, unpubl. data). In Italy, Saino et al. (2004b) found that more females started laying when temperatures in the preceding one to four days were high; other studies have recorded unusually early laying dates when temperatures were high or insects particularly abundant, or late ones in very poor weather (e.g. Radermacher 1970; Thompson 1992; Loske 1994; Brombach 2004). Current climate change is likely to increase spring temperatures and insect abundance, but the effects on laying dates of Barn Swallows are not yet clear. In Britain there is a trend for birds to begin laying earlier and this is related to climate change (Crick & Sparks 1999). For British Barn Swallows, laying dates have changed over the past few decades but in a curvilinear fashion; however, laying has been earlier since the late 1980s and an advancement of seven days by 2080 is predicted if the trend continues (Crick & Sparks 1999; Baillie et al. 2005). In contrast, Møller (2002c) did not find any relationship between laying date in Denmark and an index of weather (the North Atlantic Oscillation index, Chapter 10); neither did early spring temperatures affect the relative laying dates of Barn Swallows of different ages (Møller & Szép 2005a). Although warmer springs allow Barn Swallows to return to the breeding grounds earlier, it is the males that do so, and the timing of laying is still limited by the females’ migration schedule (Møller 2004b; Chapter 10). Breeding habitats vary in both abundance of insects and local climate, and hence in their suitability for early laying. For example, in Italy, Barn Swallows breed earlier on farms with cattle than on those without, suggesting that food is more abundant early on when livestock are present or possibly that the nest sites are warmer, reducing energy requirements (Ambrosini et al. 2002a). Laying date is not always affected by habitat, however, possibly because Barn Swallows are not tied to their nest sites so much at this stage and can feed at better sites further away than when they have eggs or chicks (Evans 2001; Møller 2001b). For individual birds, laying may depend on when they arrive and how quickly they get a partner. Long-tailed females, which are in good condition and which are generally older birds, lay earlier than short-tailed and younger ones, at least in Europe. In North America, Safran & McGraw (2004) found that colourful females laid earliest. In general the females’ body size has little or no effect on their reproductive output, but those whose partners have long tails also lay earlier (Banbura ´ 1986; Thompson 1992; Møller 1994a).

14639.qxd

24/1/06

3:53 pm

Page 115

Eggs and incubation

115

EGGS The eggs are laid early in the morning, mostly between 04:00 and 08:00 hours (Møller 1987f; Thompson 1992; Ward 1996), usually once a day, but occasionally a female may miss a day or more. These interruptions occurred in about 10% of nests in Scotland (Thompson 1992; Ward 1992). The reasons for them are not always clear. Some interruptions could be the result of, for example, disturbance or loss of the male or the female changing mates. Poor feeding conditions may also have some effect. For example, of eight interruptions of two to six days reported by Radermacher (1989), in a study in Germany, at least two were associated with cold weather. Ward (1992) recorded 13 interruptions and desertions during laying over three years, in both first and second clutches, but only three were associated with prolonged bad weather: one female resumed laying, but the other two abandoned the breeding attempt. The majority of the interruptions lasted a day but a few lasted 2–14 days. However, even those longer than a day, including the 14-day interruption, did not seem to affect hatching success. Interrupting laying probably allows the female to lay a large clutch with minimal delay, whereas abandoning a clutch and relaying could lose the female at least 12 days (Thompson 1992). Barn Swallow eggs are white with variable amounts of mainly reddish or purplish brown and some lilac and grey speckles and blotches. Eggs within a clutch, and within successive clutches laid by the same female, look more similar than do eggs from different clutches laid by different females (Møller 1987c), although the difference is slight, at least in North America (Brown & Sherman 1989). The size of the eggs is similar in different parts of the range. For rustica, egg size in 231 clutches was 17.6–21.8 × 12.8–14.9 mm, averaging 19.6 × 13.7 mm, with a fresh weight of 2.0 g (range 1.7–2.3 g; Ward 1995). For erythrogaster, egg size in 22 clutches was 16.3–21.7 × 12.4–14.8 mm, averaging 19.3 × 13.8 mm, with a fresh weight of 1.9–2.0 g (range 1.4–2.1 g; Brown & Brown 1999a). Sample sizes are small for other populations, but eggs from other races are similar in size to, or perhaps slightly smaller than, those of rustica and erythrogaster (Glutz von Blotzheim & Bauer 1985; Cramp 1988). Individual females lay eggs of similar size in successive clutches and between years, that is, some females consistently lay small eggs and others large ones (Ward 1992, 1995). Banbura ´ & Zielinski ´ (1998b, 2000) found that about two-thirds of the variation in linear dimensions and volume between eggs in their study population resulted from differences between females and that females’ egg volumes were consistent between years. Similarly, Ward (1992, 1995) reported that different females accounted for 60% of the variation in egg weight in the population. In contrast, males have little effect on the size of their partners’ eggs (Banbura ´ & Zielinski ´ 1998b). Egg size is not related to the females’ size or age, although it may reflect another aspect of their quality such as metabolic efficiency or foraging ability (Ward 1992, 1995; Banbura ´ & Zielinski ´ 1998b). Some studies have found no relation between clutch size and egg size (Ward 1992, 1995; Zielinski ´ & Banbura ´ 1998), but

14639.qxd

24/1/06

116

3:53 pm

Page 116

The Barn Swallow

Akopova et al. (2000) reported that three-egg clutches had smaller eggs than larger clutches did, whereas Pap & Szabó (1998) found a decline in egg volume with clutch size. Egg weight generally increases with the order of laying (Marks 1982; Slagsvold et al. 1984; Banbura ´ & Zielinski ´ 1995b; Saino et al. 2004b), although it did not in Ward’s study (Ward 1992, 1995). Since the eggs in a clutch hatch over a couple of days and tend to hatch in the order laid (McGinn & Clark 1978; Saino et al. 2001a), laying a large last egg may mean the last to hatch is still close in size to its older nestmates (Slagsvold et al. 1984). Environmental factors also affect egg size. Ward (1992, 1995) found that egg weight in Scotland was not strongly related to the weather or insect abundance, but there was a slight effect of maximum temperature during the females’ peak period of egg formation. In adverse weather, females seemed more likely to delay laying for a few days than produce a small egg. An Italian study (Saino et al. 2004b), however, found a stronger positive effect of temperature on egg weight, on days two to five before laying. Saino et al. (2004b) also found that the last and first eggs were most similar in weight when temperatures were high, as temperature seemed to have more effect on the weight of the first egg. In Scotland, egg sizes of females laying in different years were more strongly correlated for second than for first clutches, indicating that environmental conditions may have most effect early in the season, at least at high latitudes (Ward 1992, 1995). The weather, and its effect on the food supply, also affects the egg’s composition and quality. A typical egg is composed of 0.05 g of shell, 0.43 g of yolk and 1.19 g of albumen; the albumen is 89% water, 10% protein and 1% lipid (fat), and the yolk is 55% water, 29% lipid and 16% protein. A large egg contains more yolk and albumen than a small one and has proportionately more lipid in the yolk (Ward 1992, 1995). Ward found that insect abundance during the six days before the egg was laid explained 23–24% of the variation in the amount of lipid in the yolk and in the whole egg. Only the lipid was affected in this way, not the whole egg, yolk or albumen content. Since environmental conditions seem to have more influence on the yolk than on albumen, egg quality probably depends more on how much energy the female can get rather than how much protein. Whether variation in egg size affects breeding success is not clear. Saino et al. (2004b) found that hatchability increases with egg weight, but Zielinski ´ & Banbura ´ (1998) found no consistent relations between egg weight and laying date, hatchability or fledging success. Large eggs do produce large, heavy hatchlings (Ward 1995; Saino et al. 2001a) but hatchling weight may also depend partly on environmental conditions, because of their effect on the lipid content of the eggs. Whether larger eggs improve the survival of hatchlings is not known. Egg size may have less influence than other factors such as brood size, position of the chick in the weight hierarchy in the brood and date of fledging. Thus first-laid eggs tend to be the first to hatch and to produce large, heavy chicks, but later hatchlings catch up in skeletal size by the age of 12 days (Saino et al. 2001a). Females affect the quality of their eggs, by providing carotenoids and immune factors to boost the chicks’ immune response. Carotenoids such as lutein, which are

14639.qxd

24/1/06

3:53 pm

Eggs and incubation

Page 117

117

obtained from the diet, are important for a healthy immune system and as antioxidants. They may be involved in the development of the embryos’ immune systems and their effect may extend beyond hatching. Saino et al. (2003e) experimentally changed the carotenoid content of eggs by injecting lutein into the yolk and found that this improved the immune response of the chicks. However, females may be limited in how much carotenoid they can transfer to their eggs, since their own blood levels decline before egg-laying (P. Ninni & A P. Møller, unpubl. data in Saino et al. 2002b) and more lutein is provided to the yolks of first-laid than last-laid eggs (Saino et al. 2002b, 2003h). Furthermore, females whose immune systems have been challenged provide less carotenoid. Lutein concentrations in eggs also increase with increasing air temperature six to nine days before laying, suggesting that females can add more to the developing yolk when food is plentiful (Saino et al. 2004b). When the tail length of males was experimentally changed, their females transferred more lutein to the eggs if their mates had shortened tails than if they had elongated ones (Saino et al. 2002b, 2003h). Naturally short-tailed males may have poor resistance to parasites, may pass this poor resistance to their offspring and may expose their offspring to more parasites in the nest (Chapter 4); Saino et al. (2002b) suggested that by providing more carotenoids when they have short-tailed mates, the females improve their offsprings’ ability to cope with these parasites. Immune factors also pass from the mothers into the egg yolks. The amount of immunoglobulins in the blood of females increases before egg-laying and then declines, consistent with the notion that immunoglobulins are being transferred to the eggs (Saino et al. 2001b). Levels also decline late in the season, so second broods may have reduced immunity (Saino et al. 2001b). Females vaccinated with Newcastle disease virus vaccine transferred antibodies to this antigen to their eggs (Saino et al. 2002a, 2003h). First-laid eggs received more than later ones but only when the females were mated to males whose tails had been elongated and who thus appeared to be very attractive. Saino et al. (2002a) suggested that female Barn Swallows, which may not have enough antibodies for the whole clutch, might give at least the first of their offspring a head start when they have apparently good-quality mates (Chapter 4). The amount of antibodies transferred to the eggs was not affected by temperature during egg formation (Saino et al. 2004b) and thus may not depend on food abundance. Females mated to long-tailed males also have high levels of immunoglobulins in their blood, possibly because these females are investing more in their offspring (Saino et al. 2001b). In the experiment carried out by Saino et al. (2003h), eggs with female embryos also received more antibodies against Newcastle disease virus than those with male embryos; the researchers speculated that females are more susceptible to infection, suggested by their higher mortality after fledging (Chapter 9). However, there was no difference in lutein concentration of eggs with male and female embryos. Lysozyme, an enzyme that protects against bacteria, is transferred from the females into the albumen, with more in the first-laid eggs, and is carried over into the hatchling; high levels of lysozyme are associated with improved hatchability of

14639.qxd

24/1/06

3:53 pm

Page 118

118

The Barn Swallow

the eggs and perhaps with chick survival (Saino et al. 2003c). More lysozyme is transferred into the eggs when the air temperature is high five days before laying, again suggesting a link with food abundance for the females (Saino et al. 2004b). Finally, androgens pass into the yolks of the developing eggs; the amount varies between females, and is greater in first than in second clutches. In other bird species, androgens influence growth, begging and dominance of chicks. In Barn Swallows, Gil et al. (2005) found that high levels of androgens were associated with faster weight gain but not with chick size at 13 days, so the benefits of having high levels in the eggs are not yet clear. As for antibodies, females transferred more androgens when mated with males with elongated tails than when their partners had shortened tails. Females that arrived early also had high androgen levels in their eggs.

CLUTCH SIZE Clutch size is usually three to six eggs with only a few of two, seven or eight; clutches of four or five eggs are most frequent. Clutches of nine and ten eggs have been recorded (e.g. BTO data; Akopova et al. 2000), but it is possible that two females are involved in laying these exceptions. Some large clutches might also be the result of females relaying after a long laying interruption. For example, Maimie Thompson (pers. comm.) recorded a female that laid two eggs, interrupted laying for several days, and then laid a clutch of five eggs, to make a total of seven. For birds in general, clutches tend to be larger at higher latitudes. Various hypotheses have been put forward to explain this; the longer days or more abundant food per bird, or both of these, may allow parents to rear larger broods (e.g. Lack 1947; Royama 1969). In Barn Swallows the size of first clutches is similar in different areas but the size of second clutches increases with latitude, ranging from 4.07 in Iraq to 4.75 in Finland (Møller 1984b). Møller suggested the lack of a relation between clutch size and latitude for first clutches is because they are laid by a mixture of early, experienced and late, inexperienced females, whereas second clutches are laid predominantly by experienced females. Large second broods at high latitudes may be possible because of a combination of long days and abundant food. As in the majority of temperate-zone birds (e.g. Klomp 1970), clutch size also declines through the breeding season, both for all Barn Swallows and when the first and second broods of individual females are compared. In Scotland, for example, first clutches averaged 4.89 and second clutches 4.41 (Thompson 1992; Ward 1992; Figure 7.1). In part the decline is due to younger females laying later and producing smaller clutches (Chapter 9) but there is also a real decline with date; first broods are larger than second ones for the same parents, and size decreases with date within first broods and within second broods, perhaps because of worsening breeding conditions such as a reduction in daylight hours available for feeding at high latitudes. The

14639.qxd

24/1/06

3:53 pm

Eggs and incubation

Figure 7.1.

Page 119

119

Decline in clutch size over the season at Stirling, Scotland. Graph courtesy of Sally Ward.

decline in clutch size with date is evident for both first-years and older birds (Thompson 1992) and for both females and males. However, sometimes a female will lay a smaller first clutch, probably because bad weather early on prevented her from laying a larger one. In such cases the female may have a large second clutch (e.g. Ribault 1982). Clutch size can also vary between years and habitats, probably in relation to the food supply. In Scotland, for example, more females laid first clutches of six or seven eggs in 1989 (in a warm spring) than in 1987 and more clutches of five in 1988 (Thompson 1992). In Stavropol, Russia, the average clutch size was 4.3–4.4 in 1997–1998, but only 3.9 in 1995 (a hot, dry summer); in 1997–1998, 11% of pairs had clutches of six compared to 2.6% in 1995 (Akopova et al. 2000). An important cause of variation in the weather is the North Atlantic Oscillation (NAO; Chapter 10). In Møller’s Danish population, first but not second clutches were larger after winters with a high NAO index; as the NAO index increased, first clutches became relatively more important for fledgling production (Møller 2002c; Figure 7.2). The mild wet winter and early spring associated with a high NAO index may encourage a good insect population ready for Barn Swallows during laying. A good food supply also depends on the habitat: when Møller (2001b) compared breeding success on farms before and after they abandoned dairying, he found that first clutches were larger when cattle were present. Environmental conditions affect clutch sizes via the amount of food the females can get, as eggs are formed from current food intake rather than body reserves (Ward & Bryant 2006). During laying, the temperature and prey availability affect how much time the females spend foraging; in very bad weather they may be away from their nest sites all day (Turner 1980). Ward & Bryant (2006) found that clutch size in Scotland increased with increasing ambient temperature on the days when the

14639.qxd

24/1/06

120

3:53 pm

Page 120

The Barn Swallow

Figure 7.2. The size of (a) first but not (b) second clutches increases with increasing values of the North Atlantic Oscillation index (NAO), that is, with more favourable environmental conditions early in the year. From Møller 2002c.

eggs were deposited. The temperature during the later part of laying, when both yolk and albumen were deposited, had the strongest influence upon clutch size. Females may thus begin to grow more follicles than they ovulate, since the number of eggs laid depends upon the resources currently available. However, Saino et al. (2004b) found no relation between clutch size and ambient temperature in their Italian population. The difference between the studies may reflect differences in climate between the two areas. Clutch size is related to a number of other factors. Older females lay earlier and have larger clutches (Shields & Crook 1987; Møller 1992b; Thompson 1992; Chapter 9). Parasites also affect second clutches: Møller (1990a, 1991a) found that females that reared a first brood in a mite-infested nest laid a smaller second clutch (4.26 eggs) than did females with mite-free nests (4.64 eggs). However, the number of parasites in the nest does not seem to affect the size of first clutches directly (Shields & Crook 1987; Møller 1990a). Møller (1982) found a positive correlation between nest volume and clutch size for both first and second clutches in his Danish population. The relation varied between years, however, with significant correlations for first clutches in two years of low population density but not in peak years, whereas for second broods there were significant correlations only in peak years. The females may build a cup size appropriate to the number of eggs they will lay, rather than adjusting clutch size to nest size (Soler et al. 1998; Chapter 4).

14639.qxd

24/1/06

3:53 pm

Page 121

Eggs and incubation

121

CONSTRAINTS ON CLUTCH SIZE Experimental evidence shows that, like other species, Barn Swallows are able to incubate clutches and rear broods larger than they usually have. Why then don’t Barn Swallows lay larger clutches and rear larger broods? Clutch size does not seem to be constrained by the time or energy required of the females to incubate, at least in reasonably good conditions. Possibly, females have smaller clutches than they could normally incubate because of the risk of encountering poor feeding conditions, when they could not incubate them without losing weight. However, clutch size may be limited by other factors, as suggested by the results of experiments in which females are given artificially larger or smaller clutches or broods. Engstrand & Bryant (2002) moved eggs between nests a few days after clutch completion, so that females had their natural clutch sizes increased or decreased by two eggs, or left the same. The females’ normal clutches were returned to them at the end of the incubation period. This manipulation did not seem to affect incubation behaviour, but the incubation period was a day longer for enlarged than for reduced clutches (15.6 versus 14.8 days) and hatching success, of nests that did not fail completely, was also lower for enlarged clutches (86.7% versus 98.8%, and 91.9% for natural clutches). Maintaining optimal humidity and temperature in the nest may be a problem with large clutches. However, there was no evidence that eggs in enlarged clutches lost excessive amounts of water and Engstrand & Bryant suggested that large clutches, and especially those eggs on the periphery, might have been exposed to more variable temperatures, with adverse consequences for embryo growth and thus hatching success. The higher hatching success for reduced clutches compared with natural clutch sizes suggests that such factors may constrain clutch sizes in natural conditions. Furthermore, high ambient temperatures in the summer may harm the viability of first-laid eggs before incubation starts, making smaller clutches more advantageous for females (Stoleson & Beissinger 1999). Thompson (pers. comm.) also found that females were more likely to desert artificially small clutches and that eggs in enlarged clutches sometimes got flicked out. As well as clutch size being limited by constraints during incubation, there may be limits on the number and quality of chicks that can be reared. Barn Swallows are able to rear larger broods than they normally lay; for example, pairs given extra chicks in experiments can rear seven or eight and produce more fledglings than from normal or artificially reduced broods (e.g. Jones 1987a; Thompson 1992). However, chicks in enlarged broods are smaller, with poorer immune responses, than those from natural-size broods, so their long-term survival may be compromised (Snapp 1973; Jones 1987a; Thompson 1992; Saino et al. 1997f, 2002g). Thompson (1992) also found that more chicks died in enlarged broods, mainly because of total nest failures, especially in poor weather. Artificially enlarging first broods also delays the laying of second ones and reduces their frequency (Thompson 1992; Saino et al. 1999b; Chapter 9). Looking after large broods may have other consequences for parents such as greater exposure to parasites, poorer immune function and reduced survival

14639.qxd

24/1/06

122

3:53 pm

Page 122

The Barn Swallow

(Saino et al. 2002d; Chapter 9). Artificially large clutches and broods may therefore produce more fledglings per brood, but at a cost to the chicks and their parents. The negative consequences of large broods may be felt especially when feeding conditions are poor. Comparison of the amount of food required by a brood and its parents with the amount the latter can collect each day suggested that Barn Swallows in Scotland should have no problems feeding even a brood of seven or eight in average to good conditions (Turner 1983). In bad weather, however, feeding rates are reduced and heavy rain may prevent the parents feeding at all. Getting enough food may then be difficult, particularly late in the season at high latitudes when days are short. The females may also have less time for feeding if the chicks need extra brooding in cool weather. Although cool, wet weather is unpredictable, it can occur quite often, for example on 10–29% of days in June–August in my study. Some years can also be worse than others; in my study, 1978 was a poor year with bad weather on 28% of days in June, 26% in July and 29% in August. Environmental conditions may thus influence the optimal brood size, if females have broods of a size that they can feed adequately in an average year. In good weather, the parents can collect extra food, building up their chicks’ fat reserves (Chapter 8), which can sustain them for a day or two if the weather deteriorates. The effect of parasites may also explain why females may lay smaller clutches than they could rear. For example, large broods suffer more from parasites than small broods and large clutches thus result in fewer fledglings (Chapter 9). Females would therefore benefit by having smaller broods, as Møller (1991a) found in natural nests, and when mite levels were experimentally manipulated. Møller calculated that a first clutch of 8.5 eggs would be the most productive size if there were no mites present, but for a nest with 10,000 mites, a clutch of 4.4 eggs would produce the most fledglings. Clutch size is probably mainly determined, however, by the ability of the parents to feed their broods. Variability in weather between years may make large broods too risky, and variation in food abundance and daylength, and thus foraging time, may affect brood size seasonally and geographically. In Scotland, for example, food abundance for Barn Swallows tends to increase early on in the breeding season and the weather becomes more predictable; daylength decreases over the summer, however, leaving less time for feeding late broods and this may favour small clutches late in the season. In contrast, in areas with hot, dry summers such as southern Spain, a decline in food availability may be the factor limiting the size of later broods. Breeding entails costs, as well as benefits; for example, the effort of rearing a large first brood may reduce a bird’s ability to rear a second brood. Putting effort into rearing chicks may mean less energy and nutrients available for self-maintenance, for example for the immune system. Individuals may have to trade off these costs and benefits. Some costs of breeding depend on the ability of the bird itself; a lowquality bird may face larger costs than a good-quality bird when rearing a brood of a particular size. Other factors, such as bad weather, scarce food or the presence of parasites, are external. These will interact, so that clutch size and number of clutches may be lower for a low-quality or young female in poor weather than

14639.qxd

24/1/06

3:53 pm

Page 123

Eggs and incubation

123

in good weather, whereas an older or better-quality female may be less affected by the weather.

INCUBATION In Europe, only the female incubates. There has been only the odd report of a male sitting on the eggs (e.g. Moreau & Moreau 1939; Berndt & Berndt 1942; Wellbourn 1993); in one case in Finland, this was during poor weather at a nest on the outside of a building when the eggs might have been at risk of chilling (H. Kärkkäinen, pers. comm). I have seen males sitting on eggs twice, but for less than a minute, with the female nearby. Even when the female is apparently absent, her partner does not usually take over the incubation; on two occasions when I caught incubating females, the male just perched nearby most of the time and one flew off and returned with another female! The female, but not the male, has a well-vascularised brood patch, an area on her belly without feathers, so that when she sits on the eggs, her body heat warms them. In Russia and elsewhere in Asia, too, males do not usually incubate (Wang 1959; Komarov 2000), but in Siberia Marks (1982) observed males sitting on the eggs in 12% of pairs. In North America, males help with incubation, but to a small and variable extent (e.g. Samuel 1971b). Smith & Montgomerie (1992) found that males incubated for, on average, 9% of the time that the eggs were covered. Females stay on the nest at night, however (Ball 1983). Long-tailed males spent little or no time on incubation, whereas short-tailed males did as much as 14% of the total; females mated to high-quality males therefore do more of the incubation (Møller 1994a). Why do North American males help incubate the eggs? One explanation is that the habit in this subspecies of nesting on exposed sites such as bridges may mean that it is harder for a single bird to keep eggs warm (Smith & Montgomerie 1992). Also, North American Barn Swallows probably have less history of nesting in close association with people than do Barn Swallows elsewhere and thus may be better adapted to incubating in cool natural sites rather than in warm livestock stalls; their historical food sources might also have been less abundant or further from the nest, increasing the time the females spend away from the eggs. When incubation starts is not clear, because the females spend increasing time on the nest, from less than 40% of daylight hours when the first egg is laid to more than 60% during the first few days of incubation (Purchon 1948; Turner 1980; Marks 1982). Akopova et al. (2000) recorded females on the eggs regularly from the laying of the first egg in 12 nests, from the third or fourth egg in 22 nests, from the last egg in nine nests and after laying was completed in five nests. In North America, Samuel (1971b) noted birds on the eggs intermittently until the penultimate egg was laid. However, incubation is usually considered to start with the penultimate or last egg, sometimes with the antepenultimate one. Early incubation may help maintain the viability of the first-laid eggs in larger clutches, as these are most at risk from adverse

14639.qxd

24/1/06

124

3:53 pm

Page 124

The Barn Swallow

ambient temperatures which may affect hatching success (Banbura ´ & Zielinski ´ 1995c; Stoleson & Beissinger 1999). Banbura ´ & Zielinski ´ (1995c) also found that an early start to incubation was linked to eggs hatching asynchronously and that asynchronous hatching was more frequent in clutches of four to six eggs than in smaller ones. I recorded egg temperatures during incubation by placing a dummy papier-mâché egg containing a thermistor into the nest. For partial clutches the egg temperature was only around 17°C, but females warmed full clutches to 35.7°C (Turner 1980, 1982b). Using a similar method, with a thermistor inside a Barn Swallow’s egg, Møller (1991c) also found that the eggs are maintained at a temperature of about 35°C. When the females leave, the temperature of the eggs starts to fall, at a rate of about 0.5°C per minute, so the females must warm them again when they return. I found that the temperature dropped by several degrees depending on how long the females were away. The minimum egg temperature averaged 25°C when the females were absent; this is about the lowest temperature at which bird embryos can develop (e.g. White & Kinney 1974; Drent 1975). When the air temperature changes, the females can maintain egg temperature by changing the lengths of their incubation and feeding bouts, incubating for longer periods and staying away for shorter periods when it is cold. North American males can maintain the temperature of the eggs at about 35°C and so are effective at preventing the clutch cooling when the females are absent (Ball 1983). However, Marks (1982) found that when males in Siberia were on the eggs, temperatures were 5–7°C lower than when females were incubating. The eggs are incubated for, on average, about 60–80% of daylight time, but this percentage depends on the external temperature (Turner 1982b; Jones 1987c; Smith & Montgomerie 1992; Møller 1994a; Komarov 2000). At higher temperatures, the female can spend more time off the eggs because they do not cool as quickly. Much of this time is spent feeding, but the female will also spend longer perching near the nest. At lower temperatures, a female will also spend more time off the eggs, in this case because she must spend longer feeding to avoid losing too much weight. Jones (1987c) recorded one female reducing her incubation time from 63% to 9% after several days of bad weather and Ytreberg (1986) recorded three females incubating for only 27–50% of the time on a day with temperatures of 3–9°C and with rain and sleet. In normal conditions, the females leave the eggs to feed only for short periods, usually two to nine minutes (Purchon 1948; Turner 1980; Jones 1989; Møller 1991c), even when the males help to incubate (Ball 1983; Smith & Montgomerie 1992). Periods spent on the eggs are generally longer early and late in the day and in cold weather. In my study they varied from an average of 22 minutes at 9–12°C to ten minutes at 20–24 °C. Inattentive periods varied less with ambient temperature, except that in very bad weather females would sometimes abandon the eggs for two to three hours. Inattentive periods were also shorter nearer hatching and for large clutches (Turner 1980). Ytreberg (1986) recorded an increase in inattentive periods of females from 10–15 minutes to 20–35 minutes in cold weather; these females also abandoned the eggs for periods of 7–12 hours. Egg temperatures in this case,

14639.qxd

24/1/06

3:53 pm

Eggs and incubation

Page 125

125

recorded with an artificial egg, fell below 25°C during these prolonged absences, but all three clutches hatched successfully. It is likely that females adopt one of two strategies, either maintaining egg temperature at a high level or, if conditions are so poor that that is not possible, temporarily deserting and letting it fall to the point where the embryos stop growing (Haftorn 1988). Other reports of clutches hatching after a suspension of incubation of 11–15 hours add to the evidence that Barn Swallow eggs can withstand a short period of cold weather when the females have to forage for themselves rather than incubate (Schulze-Hagen 1969; Ribault 1982; Saussay 1993b). The feather lining insulates the eggs, so that they cool less quickly than they would otherwise do. Møller (1991c) demonstrated this by removing feathers from some nests, leaving an average of only four per nest, and adding them to others, increasing the number from an average of 34 to 61 per nest. Eggs cooled most quickly when he removed feathers, whereas when he added them, they cooled more slowly and warmed up more quickly than in control nests or in those with feathers removed. Females in this experiment maintained the temperature of the eggs by changing their pattern of incubation: they stayed away for shorter periods and sat on the eggs for longer bouts when feathers were removed, compared with nests where feathers were not removed and those with feathers added. For the latter group, females incubated for a lower percentage of time than females with a normal nest lining, although the two groups of females had similar periods on and off the nest. The presence of feathers thus probably allows the female to spend more of her time feeding without letting the egg temperature fall too much. Females adjust the thickness of the feather lining themselves, adding feathers as incubation progresses and removing them once the chicks are sufficiently well grown not to need brooding. In Møller’s experiment (Møller 1991c), females whose feathers were removed added more and those with extra feathers removed them. The incubation period usually averages 13–15 days, but the range is wide (10–20 days; e.g. Ribault 1982; Pikula & Beklova 1987; Brown & Brown 1999a; Akopova et al. 2000; Engstrand & Bryant 2002; Figure 7.3). Some of the variation between studies results from the above-mentioned uncertainty over when incubation starts and also when it ends, as the eggs sometimes hatch over two to three days. However, there is some natural variation. Although there does not seem to be a general relation between incubation period and weather, long periods have been noted when the weather has been severe enough for females to abandon the eggs temporarily and these seem to be recorded more at high latitudes. Parasites also affect incubation, lengthening the period by about half a day on average in Møller’s (1990a) study. In addition, large clutches take longer to hatch (Engstrand & Bryant 2002; Figure 7.3). The duration of incubation is important for productivity, because the longer the eggs are in the nest, the less time is available for producing a second brood.

14639.qxd

24/1/06

126

3:53 pm

Page 126

The Barn Swallow

Figure 7.3. Incubation lasts longer for large clutches. White bars: experimentally reduced clutches; shaded bars: unaltered clutches; black bars: experimentally enlarged clutches. Incubation period is days from clutch completion. From Engstrand and Bryant 2002.

ENERGETICS OF LAYING AND INCUBATION Ward & Bryant (2006) studied the development of eggs by feeding a dye to females that would stain the lipid in the developing egg. They found that each ovarian follicle develops rapidly over five days, although little yolk is put down on the first day; the albumen and shell are deposited on the sixth day, and the egg is laid at the start of the seventh day. The energy content of the material deposited in the entire clutch is greatest on the day before the first egg is laid. The peak energy requirement varies little between clutches of four to six eggs, but is 17% greater for a clutch of four than for a clutch of three. The average daily energy expenditure of 12 egg-laying Barn Swallows in Scotland was 113 kJ per day (Ward 1992), similar to that of Barn Swallows at other stages of the breeding cycle (Chapter 8); with the energy deposited as egg, total energy expenditure would be 119 kJ per day. The metabolic rate was not correlated with clutch size or the energy content of the egg, however. Ward concluded that, relative to other things that the females do at this stage, forming eggs takes only a small amount of energy and that getting enough energy should not normally limit the breeding of Barn Swallows. The females’ size had no significant effect on their daily metabolic rates in Ward’s study, nor did environmental conditions. Most of the females lost weight, apparently because they were using up fat reserves; there appeared to be no loss of protein from the pectoral muscles. The loss was small, however, only averaging 0.6 g a day, so the fat reserves did not seem to be important as a supplement to the daily diet. Given the small number of birds studied, however, such conclusions remain tentative.

14639.qxd

24/1/06

3:53 pm

Eggs and incubation

Page 127

127

The weight of females varies considerably throughout the breeding period (e.g. Loske 1990b; A.P. Møller, unpubl. data in Birkhead & Møller 1992). In Scotland, females weighed about 19 g on arrival, but gained weight especially four to five days before laying their first egg, peaking at 25 g (Thompson 1992; Ward 1992), and then lost weight throughout the laying period to reach 20–22 g when the clutches were complete, still heavier than males. The weight varied each day by 2–3 g, however, as eggs were formed and laid. The increase in weight was due to the increase in ovarian material and egg size, so that, apart from the reproductive tissue, the females’ weights remained approximately constant during the laying period (Ward & Bryant 2006). Environmental conditions had only a weak effect on fat scores and weights, but females were heavier, with more fat, during laying if the weather and food supply were good during the previous five days. Fat score and weight did not vary with clutch size in this study; however, Jones (1987a) found a positive correlation between the females’ body condition (weight in relation to skeletal size) and clutch size, and suggested that the higher fat reserves would buffer the females against the increased energy demands of reheating large clutches. Incubation is potentially costly in terms of energy, because the female has to forage actively in short periods between bouts on the eggs, reheat the eggs on her return and keep them at a temperature of about 35 °C. However, incubating Barn Swallows in Scotland had similar, but slightly lower, metabolic rates to egg-layers, averaging 105 kJ per day (Westerterp & Bryant 1984; S. Ward, unpubl. data). As for egglayers, the female’s size and environmental conditions did not seem to affect her metabolism. Ward (1992) estimated the costs of reheating eggs to be only a few per cent of the daily energy expenditure. During incubation, females maintain a high weight of about 22 g, about 2 g heavier than males at the same stage, but start to lose weight towards hatching time (Jones 1987c, 1988; Thompson 1992). During incubation, however, body weight can vary markedly from day to day and even hour to hour depending on feeding conditions. Jones (1987c) weighed incubating females by placing the nests on an electronic balance. Weights of females were most related to maximum daily temperature, being higher in warm weather. Temperature influences the abundance of insects, how quickly the eggs will cool when the females leave the nest, and how much time they spend incubating. The abundance of insects may in turn affect how quickly the females collect energy and put on weight. Jones (1987c) found a positive correlation between rate of weight change and insect abundance. In good feeding conditions, females have more time to forage, can catch prey at a higher rate and can then gain weight more rapidly (Jones 1987c). In inclement weather, in contrast, females can rapidly lose weight, sometimes to a critical level. In one case, a female lost 9% of her body weight in six hours of cold, wet weather. Another female lost 3 g between days eight and 12 of incubation when the temperature dropped from 14.5 to 10 °C, but gained 15% of her weight again on day 13 when the weather improved. Jones (1987c) found that females in poor body condition (weight in relation to skeletal size) spent less than 30% of their time, and sometimes none of it, on the eggs.

14639.qxd

24/1/06

128

3:53 pm

Page 128

The Barn Swallow

If bad weather is prolonged for several days, females will desert the nest (Ward 1992). At that point, the incubating females’ fat reserves may drop to about the same level as during late chick rearing, and their own survival may be at risk (Jones 1987c). Whether the females desert also depends on the clutch size and date: Thompson (1992) manipulated clutch and brood sizes and found that pairs were more likely to desert the more eggs or chicks were removed, when eggs rather than chicks were removed and for first than for second broods. The parents may thus abandon a small investment in breeding in favour of starting a larger one, whereas they are likely to persevere with a large investment or when the breeding season is so far advanced that they may not be able to rear another brood anyway (Dawkins & Carlisle 1976). Jones (1987c) suggested three reasons for the high weights maintained by incubating females. First, lipid stores can be used as fuel when feeding is constrained by both scarce food and high incubation demands. Second, once the chicks hatch, the females can also use their fat reserves to help maintain their weights in bad weather while they collect food for the chicks. Finally, if the females lose their clutches, they will be able to start new clutches quickly. On average, incubating females carry enough fat reserves to subsidise a day’s activity. Females in poor condition, however, would have enough reserves for only half a day (Jones 1987c).

14639.qxd

24/1/06

3:53 pm

Page 129

CHAPTER 8

Chicks and parental care All the summer long is the swallow a most instructive pattern of unwearied industry and affection; for, from morning to night, while there is a family to be supported, she spends the whole day in skimming close to the ground. Gilbert White, 1789

Once they have chicks, parent Barn Swallows spend most of the day in flight, feeding their offspring and themselves. They need to catch some 150,000 insects to rear a brood. As with other aspects of their lives, the weather and insect abundance are important in determining how quickly they catch their prey. Food is rarely so scarce that chicks starve, but their health, and potentially their survival, may be compromised by poor feeding conditions.

14639.qxd

24/1/06

3:53 pm

Page 130

130

The Barn Swallow

HATCHING The chicks within a clutch hatch over one to three days, but mostly within 24–36 hours (e.g. Radermacher 1989; Thompson 1992; Møller 1994a; Banbura ´ & Zielinski ´ 1995c). The first eggs to be laid tend to be the first to hatch (McGinn & Clark 1978; Saino et al. 2001a) but there are exceptions (e.g. Akopova et al. 2000) and, unlike some other species, there is no relation between the sex of the hatchling and laying order (Saino et al. 2002e). The female removes the eggshells and drops them several metres from the nest.

CHICK DEVELOPMENT At hatching, Barn Swallows weigh about 1.5–1.9 g. They are blind and naked apart from wisps of grey down on the back, wings and head. Although the chicks within a brood hatch at about the same time, they can vary significantly in size. In Italy, the earlier chicks to hatch within a brood weighed 2.52 g on their first day on average, whereas their later-hatching siblings weighed significantly less (1.95 g) and the difference was maintained until at least day 12 after hatching; early-hatched chicks also had longer tarsi and tail feathers at seven days (Saino et al. 2001a). A spread of hatching and of chick sizes in a brood may be beneficial to the parents; for example, if food is scarce, small chicks may die, leaving more for the others, so that the parents fledge at least some offspring when resources are limited (e.g. Ricklefs 1965; Stenning 1996). Thompson (1992) found that variation in size within a brood increased with brood size and that it was usually the smallest chicks that died. However, mortality of chicks, especially young ones, from starvation is usually low, and the large last-laid egg, the growth pattern and fat stores of chicks (see below) suggest that Barn Swallows follow a strategy of buffering their offspring against short periods of unpredictable poor feeding conditions rather than reducing brood size when food is scarce. The chicks grow most rapidly from about three to ten days of age, reaching a peak of 22–25 g on average, higher than the adult weight, when about 12–15 days old (Figure 8.1). Those chicks that attain higher peak weights grow more slowly (e.g. Languy & Vansteenwegen 1989; de Lope & de la Cruz 1989; Millard et al. 1990). After the peak weight is reached, the chicks lose weight, because the body tissues, particularly the skin and feathers, lose water as they mature; for the most part, their lean dry weight does not increase further. The pectoral muscles, however, continue to grow, increasing in lean dry weight and water content. In contrast, as food processing becomes less important, the liver becomes smaller, losing both lean dry weight and water (Ricklefs 1967, 1968b). High chick weights, above those of the adults and with subsequent weight recession, are typical of aerial insectivores and also of oceanic bird species. In these species

14639.qxd

24/1/06

3:53 pm

Chicks and parental care

Page 131

131

Figure 8.1. Growth (weight and ninth primary length) of Barn Swallow chicks in good and bad weather. From Morales Fernaz 2001.

the young birds must fly efficiently as soon as they fledge, so they have relatively long periods in the nest during which the flight muscles have time to mature fully. Ground-feeding species such as thrushes, in contrast, can continue growing after fledging, as they can get by without well-developed flight muscles (O’Connor 1984). The loss in mass before fledging may also help the young Barn Swallows to fly by increasing their power-to-weight ratio (e.g. Martins 1997).

14639.qxd

24/1/06

3:53 pm

Page 132

132

The Barn Swallow

The chicks have some fat reserves. For the first few days, these are small but they rapidly increase. Chicks that are ten or more days old have variable levels of fat. For those at, or over, the peak weight, the ratio of fat in the chicks to their fat-free dry weights is about 0.2–0.6 (Ricklefs 1967; Turner & Bryant 1979). Chicks can use this fat when food is temporarily scarce, to avoid starvation and the development of fault bars in their feathers. Chicks could probably survive a day or two on their fat reserves alone. These fat reserves are also beneficial after fledging when the young birds are learning to feed themselves. Because young Barn Swallows need to fly well as soon as they fledge, resources are concentrated into growing wings and feathers (Ricklefs 1968a, b; George & Al-Rawy 1970; Thompson 1992; Brown & Brown 1999a; Table 8.1). Pin feathers start to appear on about days four or five, and the chicks are well feathered by days 13–15. A few feathers, mainly on the back, continue to grow after fledging (Kudryavtseva 1997). The tarsi and wing bones grow most rapidly in the first six and ten days, respectively. Wing length and outer tail feather length both grow linearly until about days 28–30, but the wings reach almost adult size sooner than the tail (Chapter 1).

VARIATION IN GROWTH The rate at which chicks grow depends on how much food they are getting, so growth and body weight are affected by similar factors to those that determine feeding rates and by parasites (see p. 134). The weather has some effect, particularly when poor conditions are prolonged, affecting both the food supply and how much energy the chicks need, for example to keep warm (Figure 8.1). On days when food is scarce, broods will lose weight, especially those older than 11 days, and may die of starvation in severe weather (Jones 1987a). Egger (2000) found that the weather had most effect on growth of first broods, and insect abundance and parasites (see p. 134) on growth of second broods. During periods of poor weather chicks may also attain lower peak weights, at later ages, but Thompson (1992) found that, in general, peak weights were not correlated with food abundance, perhaps because insect abundance is usually adequate for growth. Egger (2000) also found that, except in late broods, chicks could compensate for periods of poor growth and Evans (2001) found only weak effects of the weather on growth and condition (weight in relation to skeletal size). Good habitat, however, can make a difference: chicks on farms with dairy cows weighed on average 5% more than those on the same farms when dairying was abandoned (Møller 2001b). In Evans’ study, chick condition generally increased with the proportion of grazed grass in the habitat; sites with the highest levels of grazed grassland were not beneficial, however, perhaps because of intensive farming practices (Evans 2001). Another factor potentially affecting growth is brood size. In Scotland, for example, peak chick weight declined with increasing brood size in two of three years and

14639.qxd

24/1/06

3:53 pm

Page 133

Chicks and parental care Table 8.1.

133

Development of nestling and fledgling Barn Swallows.

Age (days)

Development

1

A few tufts of down are present; no black dots (where feather quills will emerge) on the back A few black dots on the back around the thighs Numerous black dots on the back and a few around the cloaca; primary and tail feather sheaths start to emerge Numerous black dots over body, forming two rows on the breast; conspicuous primary and tail feather sheaths; alula appears as single point Black dots visible on underside of wings; sheaths on back start to emerge; ears start to open; alula appears as two bulges Eyes start to open; sheaths start to open on belly and white contour feathers protrude Follicles on back raised up from skin but sheaths not yet open Feathers on back, tail, cloacal area and alula start to appear Outermost primaries and undertail coverts appear; feathers on head and nape are rare at this age A few feathers sprout on nape; brownish feathers appear either side of bill More feathers appear on nape and below bill Nape fully feathered; bluish tint to back Face half feathered Face almost fully feathered; skin still visible on breast Face fully feathered except above bill; breast usually looks fully feathered; wing bones and tarsi reach adult size At fledging, wing length is about 80% of adult’s length but tail length is half the size of that of first-years; head-to-bill length is 96% of adult’s Inner tail length 90% of adult’s Wing is almost adult size; tail is 70% grown; keel is full size Sheaths on wings and tail gone

2 3 4 5 6 7 8 9 10 11 12 13 14 15 18–23 24 28–33 33–35

From Thomson 1992, Kudryavtseva 1997, Morales Fernaz 2001.

brood size explained most of the statistical variation in peak weight (Thompson 1992). However, some studies have found no effect of brood size on growth rate or peak weight (e.g. Languy & Vansteenwegen 1989; de Lope & de la Cruz 1989; Evans 2001). Brood size has no clear effect on the growth of wings and tails (de Lope & de la Cruz 1989; Saino et al. 1997f ). Several researchers have examined the effect of brood size by giving parents fewer or extra chicks. Such studies have found that chicks in enlarged broods have lower weights, especially compared to reduced broods (e.g. Snapp 1973; Jones 1987a; Thompson 1992; Saino et al. 1997f, 1999b, 2002g). An effect of brood size thus seems to be most evident in very large or very small broods. Brood size may also have more effect on weights in bad weather than in sunny, warm weather, so the effect may vary both within and between seasons.

14639.qxd

24/1/06

134

3:53 pm

Page 134

The Barn Swallow

Chick growth also varies over the breeding season, probably because of changes in the food supply and the number of daylight hours available for foraging. Chicks in first broods weigh more and have longer tarsi than those in second broods (Møller 1994f ). Thompson also found a decline in peak chick weight, and Evans (2001) a decline in chick condition, with date in the season. The order in which the eggs are laid has an additional effect, as the first-laid ones tend to hatch first, giving these chicks a head start. Chick weight and plumage growth thus tend to depend on the order of laying of the eggs (e.g. Saino et al. 2003e). Chick growth is also faster when the egg contains a high level of androgens (Gil et al. 2005). Parental age has some effect on chick growth. Saino et al. (2002f ) found that chick skeletal size and feather development were negatively related to their parents’ age, and the chicks of older mothers had reduced immunocompetence; chick weights also declined in relation to their father’s age after the second breeding season. In another study, pairs in which both members were older than one year had chicks with higher peak weights than those of first-year pairs (Languy & Vansteenwegen 1989). Parasites are often present in Barn Swallow nests and their numbers increase over the season so that second and third broods may suffer more than first broods (e.g. de Lope & Møller 1993a). Some, such as the tropical fowl mite, suck the chicks’ blood and severe infestations can slow development or stunt growth completely; the resulting small individuals may compete less well and have poor survival prospects (Chapter 9). Normally, however, parasites have small and variable effects on the growth of Barn Swallow chicks. In Denmark, Møller (1990a) conducted an experiment in which he fumigated some nests, infested others with mites, and left some alone as controls. He found that 15-day-old chicks in nests infested with mites weighed about 5% less than those in fumigated nests. In a Spanish population, parasites had a similarly small effect on chick weight (de Lope & Møller 1993a), and in an Italian population louse flies and mites had no such effect (Saino et al. 1998, 2002g). Chicks infested with blow fly larvae in a North American study weighed less at six to ten days old than non-parasitised ones, but then caught up with the latter, although they took longer to reach the stage of weight recession (Shields & Crook 1987). Mites appear to be an irritant, as chicks spend more time preening when mite infestations are high (Møller 1991g). Chicks in nests where mites were experimentally added preened more than those in control nests, which in turn preened more than those in fumigated nests. Perhaps to be able to fledge earlier and escape the parasites, chicks infested with parasites may grow their feathers at the expense of other body components, When Saino et al. (1998) increased the numbers of louse flies in nests, the chicks grew their tail feathers more quickly, but were in poorer condition, as indicated by low levels of blood protein and a high blood sedimentation rate, than chicks in non-manipulated broods; they also had higher white blood cell counts which indicates a response to an infection. As mentioned above, the parasites in this study did not affect the chicks’ weight and size (measured as tarsus length). Within broods, however, the chicks with the fastest feather growth had the lowest weight

14639.qxd

24/1/06

3:53 pm

Chicks and parental care

Page 135

135

gain and tarsus growth, suggesting that they put most effort into growth that would help shorten the nestling period. In contrast, Saino et al. (2002g) found that mites reduced the growth of tail feathers. Chicks differ in their susceptibility to parasites. In a study in which he crossfostered half the chicks in a brood to another nest, Møller (1990b) found that the number of mites on seven-day-old chicks was positively related to the number on their biological father at the time of his arrival on the breeding grounds and negatively related to his tail length; mite intensity on chicks was not related to that of the foster parent. In fumigated nests, without parasites, the chicks’ growth rates were similar, irrespective of their parents. The offspring of good-quality (i.e. longtailed) males thus resist the effects of parasites better than those of poor-quality males (Møller 1990b, 1997). The chicks’ ability to fight off parasites and diseases depends on their immunocompetence. This in turn depends on the conditions the chicks are reared in, for example how much food they get. Chicks in large broods, competing with many nestmates and with relatively infrequent feeds, may be under stress; they produce more of the stress hormone corticosterone which depresses the immune system (Saino et al. 2003c). Immunocompetence (as measured by the response of T lymphocytes to injection of an antigen into the chicks’ wings) is negatively related to the size of the brood but increases with body weight (Saino et al. 1997f, 2003c), so there is a trade-off for the parents between having lots of unhealthy chicks and fewer healthy ones. Chicks in large broods have both low weights and low immunocompetence: in experimentally manipulated brood sizes, chicks in reduced broods weighed more and had better immunocompetence than their siblings in enlarged broods; chicks given extra protein-rich food also had better immunocompetence (Saino et al. 1997f, 2002g; Pap & Márkus 2003). Hence chicks need both good-quality food and abundant food to stay healthy. The immune response is important because it is likely to be related to the probability of the chicks surviving to fledging (Merino et al. 2000; Saino et al. 2003e; Møller & Saino 2004). More generally, feeding conditions affect the immune response. In Denmark, the immune response of first-brood chicks relative to that of second broods was better after a winter with a high North Atlantic Oscillation index, associated with mild weather and an early spring, and probably good feeding conditions (Møller 2002c; Chapter 10). Chicks on dairy farms, which provide excellent habitat, also had a good immune response, which worsened by an average of 32% for chicks on these farms when the cattle were sold (Møller 2001b). Good feeding conditions thus have a greater effect on the chicks’ immune system than on their weight or size (e.g. Saino et al. 1997f; Møller 2002c). The level of immunocompetence of chicks varies geographically, being greater at high latitudes (Møller et al., unpubl. data in Møller 2001c). In Spain, where Barn Swallows suffer high intensities of parasites (de Lope & Møller 1993a), second broods have a larger immune response than first broods but put on weight more slowly, suggesting that they allocate resources to their immune system at the expense of growth, as expected if late-hatched young experience more parasites (Merino et al.

14639.qxd

24/1/06

136

3:53 pm

Page 136

The Barn Swallow

2000). Late first broods, of parents that have a single brood in the season, are similar to second broods in both immune response and weight gain. Brood size and parasite infestation interact, possibly via the immune system. Parasites are disproportionately more numerous in nests with enlarged broods and on chicks in such broods (Saino et al. 2002g). The depressed immunity of chicks in enlarged broods may be the cause of the greater mite infestations. The health of chicks may also be more variable in enlarged broods, with some having a very weak immune response and large numbers of mites (Saino et al. 2002g).

BROODING AND TEMPERATURE REGULATION For the first few days, the chicks cannot regulate their own temperature, so the females have to brood them to keep them warm, at about the same level as the eggs were incubated (Al-Rawy & George 1976). The females then brood at a decreasing rate during the day until they are about six to nine days old, spending shorter periods on the nest as they grow. Males will often arrive with food and interrupt a brooding period. During bad weather, however, the females brood for longer and will brood older chicks as well. The females also cover the nest at night until the chicks are about 10–12 days old, while the males may roost close by. Samuel (1971b) reported females brooding during the day until the chicks were about 15 days old and continuing to brood at night thereafter. Females spend more time brooding, and take shorter periods away, with small than large broods, as they lose heat more quickly (Turner 1980; Jones 1987a). Chicks begin to regulate their own temperature when about five days old, improving over the next week or so. In experiments at various ambient temperatures, chicks aged nine to ten days could control their own body temperatures fairly well (Al-Rawy & George 1976) and hence need little or no brooding by the females, at least during the day. At 13 days, chicks could maintain their temperature overnight as well as adults, at 39–40 °C (Al-Rawy & George 1976). Hence, by 13 days, chicks do not need to be brooded at night. By about day 15, chicks are able to control their temperature fully. At this age they are well insulated by their feathers. The adult body temperature is 40–41°C during the day, falling a degree or two at night (Al-Rawy & George 1976). The age at which chicks can regulate their temperature at this level depends on the ambient temperature. Thus, Al-Rawy & George (1976) recorded a temperature of 40 °C for chicks aged eight to ten days reared at 22–28 °C; chicks reared at 31–36 °C, however, reached this adult level by days six to seven.

14639.qxd

24/1/06

3:53 pm

Page 137

Chicks and parental care

137

CHICK BEGGING Chicks react to the parent’s shadow and contact call and will beg at artificial shadows and calls as well. For the first few days they usually do not react to a parent until it has landed at the nest, but as they grow they come to anticipate the feed and start begging vigorously in advance. By about 12 days of age they often beg before the parent arrives (Wellbourn 1993). Chicks that have just had a meal may not beg but, with increasing hunger, they will gape in the direction of the adult, stretch their necks, call loudly (Chapter 3) and stand up and jostle their siblings to get into the best position. Only one of them is fed on each visit by a parent. Begging also becomes more intense as the chicks grow, and varies with brood size and the size of the chick compared with its nestmates. Small chicks tend to beg more intensely than their larger nestmates, although the difference is not marked (Lotem 1998a, b). This is not simply a result of being hungrier, as they beg more even after being fed. Large chicks do not seem to get more than their fair share of the food, at least when food is plentiful (Wellbourn 1993). The last chicks to hatch in a brood also beg more than their early nestmates (Saino et al. 2001a). The chicks try to attract their parents’ attention with a bombardment of sound and colour. As well as calling vociferously, they beg with their mouths wide open, revealing the yellow to orange or red gape, bordered by paler yellow flanges. In addition, the gape, and especially the flanges, reflects in the ultraviolet part of the spectrum, which is visible to birds (Hunt et al. 2003). The flanges may make the chicks more detectable in the dark nest and surroundings (Kilner & Davies 1998). The ultraviolet component in particular probably makes the gape stand out from the background (Hunt et al. 2003). The gape owes part of its colour to carotenoids: more carotenoids mean a redder gape, at least to human eyes. Carotenoids are important for a healthy immune system, so a chick with an infection may need to redirect carotenoids to its immune system and so have less available for its gape, which will then appear yellow. Saino et al. (2000a, 2003b) have shown that gape colour varies with the health of the chick. They injected Barn Swallow chicks with sheep red blood cells, which are harmless but mimic a parasite infection; the chicks had less intensely coloured gapes than their nestmates six days later. However, when they were given extra carotenoids in their diet, these chicks developed bright red gapes. In addition, chicks seem to get only limited carotenoids from the diet, not necessarily enough both to combat an infection and to colour the gape. Thus Saino et al. (2003b) found that chicks in experimentally enlarged broods, which are fed less and consequently weigh less and have low immunocompetence, had less red gapes than chicks in reduced broods. A series of experiments on the begging display of Barn Swallow chicks has shown that parents respond to both the hunger and the health of the chick. These experiments involved depriving chicks of food for a short while, adding or removing a chick soon after hatching to change the brood size, and injecting chicks with sheep red blood cells (Saino et al. 2000b; Sacchi et al. 2002). Food-deprived chicks not

14639.qxd

24/1/06

3:53 pm

Page 138

138

The Barn Swallow

surprisingly begged more, both in frequency and in the length of the syllables in the begging call. The parents responded with more feeds, but only if the chicks had not been injected with the sheep cells, that is, if they were still healthy. This finding suggests that the parents respond to the chicks’ general health and condition as well as to their immediate need for food. Chicks in enlarged broods, however, did not beg more, so although in generally poorer condition they were not necessarily motivated to beg. In addition, parents of enlarged broods did not respond to how hungry or healthy a chick was, possibly spreading food more evenly among the chicks when faced with so many. Parents appear to judge how hungry the chicks are from the intensity of their begging. Heavier chicks have lower-frequency calls than lighter ones, so parents may be able to assess the chicks’ condition from their calls, but gape coloration seems to be of particular importance. When the researchers altered the gape colour of chicks they found that the parents preferentially fed chicks with red rather than yellow gapes. So parents seem to concentrate their efforts on the chicks that are already healthy and have a good chance of survival. However, parents do not ignore any of the brood. Over a day, chicks in a brood each receive similar amounts of food, partly because after being fed a chick takes time to defecate, and so its broodmates have the opportunity to get a meal, and a pair of Barn Swallows usually manages to fledge all their chicks. Thus the parents may provide a certain amount of food to all the chicks, feeding on a ‘first beg, first feed’ basis, and then give extra, if available, to the healthier chicks (Saino et al. 2000b). Although there is competition between chicks to get food from the parents, it seems to be the parents that choose whom to feed. We do not know yet what a Barn Swallow sees as it approaches its brood. These experiments were done in good light conditions and with human-visible colours, ignoring ultraviolet. It may be that the ultraviolet component enhances the contrast between the gape and the flanges when the gape is redder and this may make the chick stand out more.

FEEDING RATES Male and female contributions There have been rare reports of males passing food to the females at the nest, the females either eating it or giving it to a chick (e.g. Owen 1918; Jenner 1945; Hosking & Newberry 1946; Purchon 1948), but normally both males and females feed the chicks directly. Within pairs, the male’s share is often slightly less than the female’s (e.g. Turner 1980). In Denmark for example, males contributed 46% of feeding visits on average for both first and second broods (Møller 1994a) and in Italy males fed about 10% less than females (Saino & Møller 1995b, unpubl. data in Saino et al. 2002f ). The male’s contribution varies considerably between pairs, however (Figure 8.2).

14639.qxd

24/1/06

3:53 pm

Chicks and parental care

Page 139

139

Figure 8.2. Male Barn Swallows vary in their contribution to chick feeding (the percentage of total feeds by males and females in different pairs). From Møller 1994a by permission of Oxford University Press.

Until the chicks are about eight days old, the number of feeding visits by each parent is variable. The females usually bring food each time they come to the nest, but will also come just to brood the chicks, especially recently hatched ones, and the males may do most of the feeding for the first few days, while the females are brooding. For older chicks, feeding rates are less variable (Jones 1987b) and, as the chicks grow, males and females bring food at similarly high rates (Jones 1988). In addition to collecting slightly fewer meals, males also collect smaller ones than females do, while among females, structurally larger birds (i.e. with longer keels) collect larger boluses (Jones 1987b). Differences in bolus size between individuals, and between days for the same individuals, are generally small, however, so the amount of food delivered to the nest depends mainly on the parents’ feeding rates (Jones 1987b). Males seem to vary more in their commitment to broods than females do. For second broods, in some pairs the males alone increase their feeding rates, in some both the males and females do so (Waugh 1978; Turner 1980) and in others males feed second broods less overall than first broods (Møller 1991i). However, Thompson (1992) noted a male continuing to feed an enlarged brood of eight, to the point of starvation, while the female deserted to start another brood with a different male. Both parents are usually required for the nest to be successful, although females will partially compensate for absent males and there are cases of a single male or female successfully feeding and fledging a brood (e.g. Radermacher 1970; Crook & Shields 1985; Møller 2000). Some of the variation in feeding rates of males and females depends on the quality of the males. The males that females prefer, those with long tails, seem to do the least work, while their partners do more (Chapter 4). Another factor affecting the males’ feeding rate is their level of blood testosterone. High levels of this sex

14639.qxd

24/1/06

3:53 pm

Page 140

140

The Barn Swallow

hormone are known to depress parental behaviour in a number of bird species, including Barn Swallows. Males experimentally implanted with testosterone fed their chicks only half as frequently as other males did (Saino & Møller 1995b). Their females compensated almost completely, so the chicks were not fed less overall and survived just as well.

Brood size and age The age and size of the brood together are the most important factors determining how much time the parents devote to foraging each day (explaining a third to a half of the statistical variation in my study), and also strongly affect feeding rates, i.e. the number of feeds brought to the nest per hour (explaining about 20% of the variation; Turner 1980). In Scotland, a one-day-old brood of five were fed an average of six times an hour, compared with 17 times an hour at six days and 29 at ten or more days (Turner 1980). The best measure of food requirements, however, is brood mass to the power 0.667 (brood mass0.667 g); this relationship allows for huddling in large broods which reduces the energy needed just to keep warm. Feeding rates increase with brood size, although each chick in a large brood still receives less food than one in a small brood, because bolus sizes do not vary with brood size (Saino et al. 1997f, 2000b; Figure 8.3). Feeding rates also increase until about halfway through the chick-rearing period and then level off or decrease. The peak of

Figure 8.3. Barn Swallow chicks in larger broods receive less food than those in small broods. Feeding rate is number of feeds per hour. Vertical lines represent standard errors of the mean. Numbers of broods per brood size are shown. From Saino et al. 1997.

14639.qxd

24/1/06

3:53 pm

Page 141

Chicks and parental care

141

food requirements varies though, for example, 8–13 days in the study by Snapp (1976) and 9–16 days in that of Waugh (1978). The amount of food delivered to the chicks varies in a similar way to the feeding rates. Bolus size does not vary with the number of chicks in a brood (Waugh 1978; Turner 1980; Jones 1987b), but changes with their age. It increases during the brooding period until the chicks are about eight days old, so older chicks receive both more and larger meals. Very young chicks probably need small boluses that are easy to swallow; the parents rarely split a bolus between chicks and then only for chicks of one or two days old. For chicks older than about eight days, bolus size remains constant or declines slightly (Jones 1987b; Loske 1992).

Time of day Feeding rates vary during the day, generally being low early in the morning, peaking late morning to early afternoon, and falling in the evening (e.g. Turner 1980; Zielinski ´ & Wojciechowski 1999; J.J. Cuervo & A.P. Møller, unpubl. data). However, not all studies have found significant diurnal variation (Møller 1988c) and a study in Badajoz, Spain, recorded high feeding rates in the early morning and late evening with a lull during the hottest part of the afternoon (A.P. Møller & F. de Lope, unpubl. data in Møller 1995). In part, changes in feeding rate mirror the activity of the birds’ prey (Lewis & Taylor 1965; Waugh 1978). Although Barn Swallows are active around sunrise, they may not start feeding the chicks until the temperature rises and insects become active, particularly early in the season. They usually continue feeding until near sunset, although artificial sources of light may allow them to catch insects after dark (e.g. Knox 1992; Bulgarini & Visentin 1997).

Second broods Second broods are fed more than first broods, especially in the afternoon and evening (Turner 1980). In Scotland, for example, second broods received an average of 32 feeds per hour versus 27 for first broods. However, this does not mean that second broods receive more food, as the size of each meal decreases during the season and fewer daylight hours are available for feeding at high latitudes (Waugh 1978; Jones 1987b). Second broods are usually smaller than first ones so require less food overall.

Weather and food availability The most important factor affecting feeding rates is the availability of food, explaining a third of the variation in feeding rates in Scotland (Turner 1980). Both males and females bring food to the nest at a greater rate when insects are abundant and males may then deliver food at a higher rate than females (Turner 1980; Jones 1988). It is likely that the parents take advantage of any good weather to collect as much food as possible and so increase their own and their chicks’ fat reserves; both adults and chicks gain weight on days with abundant food (Jones 1987a). Cool, wet and

14639.qxd

24/1/06

3:53 pm

Page 142

142

The Barn Swallow

windy weather can reduce feeding rates, and prolonged heavy rain, especially with low temperatures, can stop parents feeding chicks altogether (Turner 1980). Hot weather may also limit feeding, if there is a risk of the parents overheating, or if their prey becomes too active and difficult to catch (Møller et al. 1995a). Food availability may also be determined by the number of birds feeding over the same area: Møller (1987d) found that feeding rates were lower for group pairs than for solitary ones (20 versus 30 per hour), suggesting that fewer insects were available for groups. Males and females differ in their response to bad weather and scarce food, however. Both decrease the level of chick-feeding, but males do so more than females; females make more feeding trips, deliver more food and invest more time in feeding the chicks in bad weather (Turner 1980; Jones 1987b, 1988). Jones (1988), using an index of investment (the ratio of adult body weight to food delivery rate), showed that males invested relatively more in self-feeding than in chick-feeding than females did when food was scarce; they also lost less weight in these conditions. Males may be less efficient at foraging than females because of their longer tails; or they may value the brood less because they are uncertain of their paternity or because they have fathered chicks in other nests.

Parasites Individual feeding rates may also depend on the presence of parasites in the nest. Although feeding rates did not vary in relation to natural levels of mite infestations, Møller (1994b) found that both parents fed at a higher rate when their nests were fumigated than when their nests contained mites, but only for pairs that had a single brood; for a given brood size and weight, double-brooded pairs fed their first brood at a similar rate regardless of the numbers of mites. Møller suggested that some birds are better able to cope with the harmful effects of mites and this may affect their ability to rear more than one brood. Saino et al. (1998) also found no effect of louse flies on parental feeding rates.

SEX ALLOCATION Parents are thought to bias their investment in sons or daughters according to the costs and benefits of rearing offspring of a particular sex (e.g. Sheldon 2000). For example, females mated to attractive males may concentrate on rearing sons who will also be attractive and successful at breeding. Whether Barn Swallows favour one or the other sex when feeding chicks is not known. Male and female chicks look the same and, until late in the chick period, also sound the same (Chapter 3), so it seems unlikely that parents do differentiate between them. However, there are some interesting differences in the sex ratio of chicks in relation to parental age and quality. Females have more daughters as they get older (Saino et al. 2002e). Because the breeding performance of females declines with age (Chapter 9), Saino et al. (2002e)

14639.qxd

24/1/06

3:53 pm

Page 143

Chicks and parental care

143

suggested that older females may lay female eggs if these are less costly to produce than male eggs. It is not known, however, why male eggs should be more costly. The researchers also found that females that mated with different males in successive years increased the proportion of sons they had when they mated with relatively long-tailed (high-quality) males. The sons of long-tailed males are likely to be attractive to females, just like their fathers; hence it may pay such parents to skew the sex ratio of their brood to favour males, although it is not clear whether the effect is via the male or the female or what mechanism causes the skew (Saino et al. 2002e). In addition, small broods contained more males than large ones did, and broods contained more males when there was early egg or hatchling mortality, perhaps suggesting a difference in survival or egg quality for males and females (Saino et al. 2002e).

BEHAVIOUR IN THE NEST Both parents remove faecal sacs, sometimes eating those of young chicks or dropping them several metres away. Young chicks will shuffle to face into the nest so that the parents can easily reach and remove the faecal sacs. The parents continue to remove faeces late into the chick-rearing period. However, after five to six days the chicks begin to defecate out of the nest and by the time the chicks are about 12 days old they deposit most faeces below the nest. Recent hatchlings gape when anything approaches the nest, be it a parent or a predator, but older chicks hide by flattening themselves in the nest when they hear an adult’s alarm call. They flap their wings when about nine days old and preen themselves from about day 12. By the time they reach their peak weight they are quite active and will clamber up on to the nest rim; if disturbed they may fledge prematurely.

NEST DEFENCE Both males and females aggressively defend their nest against predators and also against conspecifics (Chapter 5). Parents give alarm calls when a predator approaches the nest and will mob it if it comes too close, flying in a circle or figure of eight, diving at its head and sometimes hitting it. They approach predators more closely than do other colonial hirundines (Brown & Hoogland 1986). Other individuals, both parents and non-parents as well as juveniles, may join in the attack, but individuals and pairs usually mob predators near their own nests, so mobbing is not necessarily done by the group as a whole (e.g. Snapp 1976; Shields 1984b). Indeed, Shields (1984b) found that it was the nearest neighbours of the pair whose nest was threatened who were most likely to join in the mobbing, and these could just have been

14639.qxd

24/1/06

3:53 pm

Page 144

144

The Barn Swallow

defending their own nests. In addition, while individuals whose nests were threatened would physically attack the predator and utter conspicuous alarm calls, other Barn Swallows would silently circle overhead away from the danger, and some would just watch even when the predator was close to their own nest. Getting close to the predator is dangerous: Møller (1991h) recorded three actively mobbing Barn Swallows being taken by Eurasian Sparrowhawks and two by cats, and Møller & Nielsen (1997) noted that 11 of 15 successful attacks by Eurasian Sparrowhawks on Barn Swallows were on birds that were mobbing. The parents respond to predators more intensely as the nesting cycle, for both first and second broods, progresses from before the eggs are laid to when the chicks fledge (Smith & Graves 1978; Møller 1984a; Shields 1984b). Incubating females may at first just remain alert and then are likely to slip away quietly from the nest if a predator gets close, but parents with well-grown chicks will dive at an approaching human or other potential predator (Møller 1984a). Males and females differ somewhat: Møller (1984a) found that females are more active in defending the nest than males especially before the chicks hatch. Males defend first and second broods equally but females defend second broods less intensely (Møller 1991i). Females with a single small brood also defend the nest less aggressively than double-brooded females and first-years do so less than older birds. However, Shields (1984b) found that North American males and females were equally likely to join a mobbing group, and males within a group mobbed more intensely than females, especially during the chick-rearing period. The differences in mobbing at different stages of the nesting cycle may depend on how the parents value the clutch or brood. Clutches laid early in the season, for example, can be easily replaced, whereas if chicks are lost, the parents may not have time to breed again. How intensely males mob may depend on how certain they are of their paternity (Chapter 5). Males may also mob to protect their mates as well as the nests; they are less likely than females to find replacement mates because there are usually more males than females in a breeding population.

FLEDGING The chicks fledge when about 18–23 days old, the average in my study being 21.1 days (Turner 1980). The average for Britain is also 21.0 days (range 16–26 days, BTO Nest Record data, Crick et al. 2003). There seems to be no or little geographical variation: in a study in Virginia, USA, the average was 20.7 days (range 18–27 days, Samuel 1971b) and in the southern part of the species’ range in Spain it was 21.2 days (range 18–25 days, de Lope Rebollo 1983). Shorter periods down to 14 or 15 days have been reported but early fledging may be caused by disturbance at the nest (e.g. Géroudet 1961; Anthony & Ely 1976). The chicks in a brood often fledge on the same day but some do so over a few days. Radermacher (1970) recorded 28 broods fledging over one day, six over two days, four over three days and one over

14639.qxd

24/1/06

3:53 pm

Chicks and parental care

Page 145

145

four days. In those broods where hatching, fledging or both occur over a few days, the day of fledging can be difficult to determine, especially when fledglings at first perch near and then go back to the nest. This may account for some of the longer fledging periods recorded. Some parasites can shorten the time that chicks are in the nest. As mentioned above, chicks may hasten the growth of their feathers so that they can escape the attention of parasites in the nest. Møller (1990a) found that first-brood chicks fledged significantly sooner at 20.5 days in nests where he had added mites compared with 22.0 days when nests were fumigated to remove mites; the times for second broods were 19.5 and 21.0 days respectively. In contrast, chicks infested with blow flies took longer to fledge (22 days) than non-parasitised ones (20 days), perhaps because of poorer growth overall (Shields & Crook 1987). Other factors affecting growth, such as food availability, may also delay or hasten fledging. The fledglings stay fairly near the nest site for about a week, usually in a tree, on a wire or other secluded spot, and usually away from other Barn Swallow families, (e.g. Thompson 1992), but the brood may be split up, with each parent tending to look after certain fledglings (Møller 1991i). Medvin & Beecher (1986) found that parents took their fledglings to sites on average 0.48 km from the nest. The family stayed at the site; if a fledgling left, it was nearly always with a parent. Families were near other families only 11% of the time and hardly at all for the first couple of days. The families gradually became more mobile and the researchers recorded both single fledglings and some mixing of families a week after fledging; by the end of two weeks the family groups had gone. Families often stay together for three to four weeks after fledging, however; in one case for two and a half months (Cramp 1988). The fledglings remain quiet until a parent approaches with food, when they start fluttering their wings and calling vociferously. The call and movements may help the parent locate the youngsters among foliage. When just out of the nest, fledglings are usually fed on their perch, but later they often fly up to meet the adult, hover in front of it and are fed on the wing. Fledglings are fed by the parents for several days, on average about five to seven days and up to about 10–12 days (Medvin & Beecher 1986; Møller 1991i; Thompson 1992). Fledglings usually roost at the nest site, sometimes in the nest or in the building, or in vegetation outside, for a week or more, in one case for 40 days (Radermacher 1970). First-brood fledglings will often be around when the female starts her second one, and may still roost with the female or in the nest even if there are recently laid eggs in it (e.g. Radermacher 1989; Thompson 1992). The first brood sometimes remain with their parents for longer, while the second clutch is being incubated or the brood is being fed (e.g. Berndt & Berndt 1942; Myers & Waller 1977). However, males may also chase their first brood off when a second clutch is laid (von Vietinghoff-Riesch 1955; Cramp 1988). As well as learning to catch insects themselves, fledglings will ‘play’ with nesting material such as grass stems and feathers, dropping and catching them in flight (e.g. Radermacher 1970; Thompson 1990), sometimes carrying them to the nest; this behaviour probably accounts for reports of first-brood fledglings helping their

14639.qxd

24/1/06

3:53 pm

Page 146

146

The Barn Swallow

parents build a nest for a second brood (e.g. Jenner 1945). There were also early reports of first-brood fledglings feeding the second broods of their parents, but the identities of these birds have rarely been confirmed and later studies have identified many visitors to nests as adults with usually less altruistic reasons for being present (e.g. Myers & Waller 1977; Crook & Shields 1987; Medvin et al. 1987; Chapter 5). Birds identified as juveniles in early reports may sometimes have been first-years that still had juvenile-like plumage (Medvin et al. 1987). Juveniles often enter buildings where other pairs of Barn Swallows are nesting (e.g. Thompson 1992; Wellbourn 1993). They will roost with other families of similar age (M. Thompson, pers. comm.) and they sometimes get into other pairs’ nests with younger chicks and are fed by the nest owners, which do not distinguish between their own offspring and others, and are not usually aggressive to those of other pairs (e.g. Ball 1982; Cramp 1988; Chapter 3). Fledglings are particularly likely to land in other nests during prolonged bad weather when it is difficult for them to feed. In such circumstances, occupied nests are likely to provide warmth as well as possible food. In one case the intruders covered the younger chicks and prevented them from being fed (Zielinski ´ & Banbura ´ 1995). When they reach independence, juveniles may move away from their natal site, apparently wandering rather than starting out on migration (Chapter 10). However, some families are still together when it is time to migrate and appear to leave at the same time, whereas in other cases one or more juveniles or adults will stay on longer than the rest of the family (e.g. Radermacher 1970). It is not known how often families migrate together; however, there are records of juveniles still being fed while on migration (e.g. King 1988).

ENERGETICS OF BREEDING In general, females use their fat reserves and lose weight from late incubation throughout the brooding period and then remain at a more stable weight, of about 18–19 g in Scottish birds, when chicks require the most feeding, although the pattern is variable (Jones 1987a; Thompson 1992). Large fat reserves are needed early on because the females can use them when their feeding time is constrained by the demands of incubating eggs or brooding chicks, especially in bad weather when food is scarce. However, when females are spending most of the day catching insects to feed chicks they need to reduce the energy costs of flying, so a lower weight may then be optimal (Norberg 1981; Moreno 1989). This weight loss appears to be a ‘programmed anorexia’ rather than a response to the energy demands of both brooding and feeding chicks (Jones 1987a). Females could save about 6% of their daily energy requirements during peak chick-rearing by losing about 6% of their weight during brooding; in addition, fat lost during brooding would provide 6% of the daily energy requirements at that time. Females appear to target their weight loss to an optimum and reach a similar

14639.qxd

24/1/06

3:53 pm

Chicks and parental care

Page 147

147

weight to males by the end of the brooding period. Those ending incubation at a low weight gain weight to reach this optimum. By the end of the chick-rearing period, females would on average carry enough fat reserves to subsidise two-thirds of their daily energy expenditure (Jones 1987c). Males have more constant weights during the early stages of breeding, but also generally lose some weight at the beginning of chick-rearing (Jones 1987a; Thompson 1992). Weights of both parents also vary from day to day, however, falling when food is scarce and when the birds deliver food to the chicks at a sustained high rate (Jones 1987a). In bad weather, while both parents may lose weight, females seem to lose more than males, in line with their greater commitment to feeding the chicks (Jones 1988; Loske 1990b). As well as losing weight while breeding, males and females also lose protein reserves. Thompson (1992) found that the breast muscles of Barn Swallows were largest before laying and during incubation, but were thin when chicks were being fed. Although the loss of weight may have advantages, the exertions of chick-rearing do seem to affect the health of Barn Swallow parents. Thus, white blood cell counts indicate that the health of early-breeding males decreases over the season; in contrast, late-breeding females, which expend less effort overall, improve their condition from prelaying to chick-rearing (Pap 2002). When they experimentally increased or reduced broods by one chick, Saino et al. (2002d) found that males with reduced broods had a better immune response than those with normal or enlarged broods, suggesting that they were less stressed. Pap & Márkus (2003) found a similar increase in immune response for females with experimentally reduced broods. Because individuals may lose condition as a result of rearing offspring, those in better condition on arrival may be better able to start breeding earlier and thus invest in larger and more broods than those in poorer condition (Pap 2002). Some researchers have used the doubly labelled water technique to measure the energy expended by Barn Swallows while breeding. This technique involves recording the turnover rates of isotopes of hydrogen and oxygen in the bird’s body, from which the respiratory rate, and hence energy used, can be calculated. In Scotland, Westerterp & Bryant (1984) found that males had higher daily energy expenditures than females (111 and 108 kJ per day, respectively), even though the males fed the chicks less. Energy expenditure was higher later in the breeding season and for birds that spent more time flying; it was low for birds that lost weight, possibly because these birds relied on fat reserves and spent less time foraging. In Switzerland, males and females had similar daily energy expenditures (114 and 112 kJ, respectively), which increased with increasing age and size of the brood (L. Schifferli, pers. comm.). In contrast, Nudds & Spencer (2004, pers. comm.) measured daily energy expenditures averaging only 69 kJ per day for males feeding chicks in Scotland. In Spain, males also had higher daily expenditures than females (90 kJ versus 85 kJ; Cuervo et al. 1996a). The reasons for the different expenditures obtained in these studies are unclear. Females take their own body condition into account when feeding chicks. Spencer & Bryant (2002) changed the energy status of females with chicks aged 10–14 days by keeping them overnight at either 29°C or 7°C and measuring their

14639.qxd

24/1/06

148

3:53 pm

Page 148

The Barn Swallow

energy expenditure. Females at the lower temperature would be predicted to use up more energy to keep themselves warm and would start the day with low reserves, whereas the warmed females would have energy to spare. The warmed females brought food for the brood more often (a mean of 18 times per hour) relative to control females (11 times per hour) kept at the ambient temperature, whereas chilled females visited the nest less (four times per hour). Warmed females also increased their energy expenditure during the day (to 66 kJ) and chilled females decreased theirs (to 28 kJ), whereas control females had an energy expenditure of 53 kJ. Females thus responded to a surplus or deficit of energy by putting more or less effort, respectively, into feeding their broods.

14639.qxd

24/1/06

3:53 pm

Page 149

CHAPTER 9

Productivity and survival In the spring of 1876 snow squalls and frosty weather held until late in June. The poor [swallows] had had no opportunity to recover their exhausted condition, resulting from their long flight to the north. Many of them succumbed to the chilling weather, while others, benumbed by the cold, permitted themselves to be handled and seemed to enjoy the warmth given out by the hand. Lucien Turner, 1886

Barn Swallows usually breed fairly successfully. In general, few nests fail completely, about 90% of eggs hatch and 80–90% of chicks fledge, although some studies have reported low success over several years, for example because of predators, bad weather or, especially in North America, House Sparrows (e.g. Alatalo 1976; Snapp 1976; Jarry 1980; R.J. Safran, pers. comm.; Table 9.1). However, there is much variation between years, between pairs and between individuals. Exactly how many fledglings, and eventual recruits to the breeding population, a pair of Barn Swallows

14639.qxd

24/1/06

3:53 pm

Page 150

150

The Barn Swallow

produce depends on many factors. Some of these are characteristics of the birds themselves, such as their age, size and quality; others are environmental, such as nest competitors, parasites, predators, weather and habitat. Most importantly, more fledglings can be reared when there is time and resources for a pair to have more than one brood per year.

SECOND BROODS Many pairs will have a second or even a third brood in a season (Table 9.1). The percentage having two broods depends critically on how early pairs lay (Møller 1994a,f ); late pairs never have two, whereas the earliest may have time for three. Within Europe, relatively fewer second clutches are laid at higher latitudes and third broods are generally uncommon, with most studies reporting none or their occurrence in only 1–3% of pairs (Møller 1984b). Third broods have been recorded most frequently in southern Europe (12.8% in Spain, de Lope Rebollo 1983; 13.3% in Italy, Brichetti & Caffi 1992; 32% in Sicily, Dimarca & Lo Valvo 1987). In North America, Barn Swallows are not known to have successfully reared more than two broods (Brown & Brown 1999a). Pairs rearing more than one brood usually produce more fledglings per year than single-brooded pairs (Møller 1990d; Thompson 1992). As well as having an extra brood, double-brooded females are likely to have larger first clutches than singlebrooded females, because clutch size declines with time during the breeding season and single-brooded females are likely to lay later. The size of the first brood may affect later productivity, however, perhaps via the effort involved in rearing it. Thompson (1992) found that pairs that had reared an experimentally reduced first brood reared more fledglings in the second, because of low chick mortality, than pairs with non-manipulated or enlarged broods. Pairs that had had an enlarged first brood were more likely to be completely unsuccessful in their second attempt (26% failed) than non-manipulated pairs (18% failed) and those with reduced first broods (5% failed). In addition, pairs that had reared experimentally enlarged broods less often attempted a second clutch (66% versus 85% for non-manipulated and 80% for reduced broods). Certain birds are more able to have two broods than are others. As well as characteristics such as tail length (Chapter 4), age is important. In Scotland nearly all older females were double-brooded but only two-thirds of first-years were (Thompson 1992). In Denmark, females two or more years old were also more likely to have a second brood (68% versus 54% for first-years; Møller & Szép 2005a). Thompson (1992) also found that females were more consistent than males in the number of broods they had between years. Parasites in the first-clutch nest slightly depress the frequency of second broods (Møller 1990a), but can have a greater effect on third broods. In Spain, where third broods are relatively frequent, de Lope & Møller (1993a) fumigated nests to

14639.qxd

24/1/06

3:53 pm

Page 151

Productivity and survival Table 9.1.

151

Examples of hatching and fledging success, the percentage of pairs with two or more broods and the number of fledglings per pair per year in various studies of Barn Swallows.

% Eggs hatching 1st/2nd broods

% Chicks fledging 1st/2nd broods

% Pairs Fledglings/ with 2 pair per or more year broods

No. of pairs

Locality

Source

not given 74.6/74.6

55* 92.3/95.4

6 34

3.4 4.8

67 544

Finland New York State, USA New York State, USA N Scotland

Alatalo 1976 R.J. Safran, pers. comm. Snapp 1976

not given

78.5*

49

5.6

301

not given

81.8*

47

5.9

150

84.5/89.7 88.0 not given 92.2/93.0

76.4/83.0 87.4 not given 89.1/82.9

62 72 75 84

6.1 6.4 6.4 6.5

1553 176 771 126

92.6/94.8

81.6/88.4

74

6.7

526

France England Germany Central Scotland Germany

88.3/87.1 90.2/95.6 92.8/92.9 not given

86.8/89.2 95.2/92.7 87.0/92.3 92.3

92 66 46 80

7.1 7.4 6.5 7.6

64 † ‡ 351

Switzerland Denmark Denmark Spain

91.7/100.0

96.5/94.5

70

7.8

30

Italy

94.5/96.1

94.2/91.8

92

7.9

56

Sicily

Butterfield & Ramsay 1998 Jarry 1980 Evans 2001 Brombach 2004 Thompson 1992 Loske 1989, 1994 Egger 2000 Møller 2001b Møller 2001b de Lope Rebollo 1983 Brichetti & Caffi 1992 Dimarca & Lo Valvo 1987

*% Eggs producing fledglings. 15 farms with cattle. ‡ 15 farms without cattle. †

exterminate parasites; 15% of pairs whose first-clutch nest was fumigated, and 29% of pairs all of whose nests were fumigated, had a third brood compared to only 8% of pairs with parasite-infested nests. The frequency of second and third broods varies markedly between years and habitats, probably mainly because of variation in the weather and the food supply, which determine when the Barn Swallows arrive, when they are able to start laying, and their ability to continue breeding during the summer (Chapters 7, 10). Thus the percentage of pairs with second broods in a German study varied over a ten-year period from 60% in a year with poor weather to 83% in a warm summer (Brombach 2004), and in a North American study over five years from 17% to 47%, with more

14639.qxd

24/1/06

152

3:53 pm

Page 152

The Barn Swallow

in summers with warm, dry weather (R.J. Safran, pers. comm.). As an example where habitat was important, second broods in Denmark were more frequent on dairy farms than on the same farms when dairying was abandoned (Møller 2001b; Table 9.1). Second broods will be started only if there is sufficient time left after rearing the first. It takes about seven weeks to rear a brood from the time the first egg is laid (Møller 1991i). Various factors can affect the time between clutches, the most important probably being whether the pair can re-use the nest they used for the first one; and a likely reason for changing nests is the presence of parasites (Chapter 6). In his Danish population, Møller (1990a) recorded the interval between the laying of the first and second clutch for pairs with first-clutch nests in three conditions: nests to which he added mites; fumigated, mite-free nests; and non-manipulated nests. The interval between clutches was shorter, at 46 days, when no mites were present than for non-manipulated nests (50.5 days) and for nests with mites added (50.3 days). The added mites forced more birds to use a different nest for their second brood (67% versus 23% of pairs with fumigated nests); however, only 30% of non-manipulated pairs used new nests suggesting that the delay in laying again was due not only to moving nests but perhaps also to an adverse effect of the mites on the parents’ condition. In a Spanish population, there was a similar, though smaller, effect of parasites on the interval between clutches, but no tendency for parasites to force pairs to build new nests for the second brood, probably because dry weather late in the season makes mud scarce anyway (de Lope & Møller 1993a; A.P. Møller, pers. comm.). Shields & Crook (1987), in New York State, found that pairs with nests containing blow fly larvae also started their second clutches ten days later. The effort involved in rearing the first brood may also affect the timing of the second. Thompson (1992) found that the interval between broods increased with brood size and, in one of three years, it decreased with increasing peak chick weight. Parents rearing broods that were artificially reduced by one to three chicks took five days less to start the second clutch than those with natural broods or parents with broods enlarged by one to three chicks. In three nests with reduced broods, the female even started to lay the second clutch before the first brood had fledged. Saino et al. (1999b) also found that parents rearing artificially enlarged broods, with one extra chick, took a few days longer (57.4 days between clutches) to start their second than parents with first broods reduced by one chick (54.7 days). The effect of brood size on the interval between broods is thus slight and seems to be greater with small than large broods. Females may also need time to recover their condition before laying a second clutch. Thompson (1992) found that double-brooded females weighed more than single-brooded ones after the first clutch, suggesting that they were in a better condition to start another brood. However, there may be an upper limit to how long females can wait: if they wait too long they may not have enough time to rear the next brood and the survival of the second-brood fledglings may be compromised (Grüebler & Naef-Daenzer 2003).

14639.qxd

24/1/06

3:53 pm

Page 153

Productivity and survival

153

PARENTAL CHARACTERISTICS Some apparent age-related effects on reproduction may be partly because of birds both reproducing poorly and dying young. However, studies that have followed individuals over a number of years have also found changes in reproductive performance, clutch size and number of broods. Date of laying, in particular, is strongly related to age. Breeding success might be expected to increase as birds age, as they gain experience. In addition, as the likelihood of surviving to the next breeding season decreases each year, birds may put their effort into breeding in the current year at the expense of future breeding attempts (Newton 1989). At a certain age, however, the bird may be unable to maintain a high breeding performance. Barn Swallow parents, especially females, seem to invest heavily in their first season’s offspring, and this may be at the expense of the quality of future offspring (Saino et al. 2002e,f ). Females’ high investment in egg production and feeding chicks, in particular, may affect their subsequent viability and reproductive performance (Saino et al. 1999b, 2002f ). Older females lay earlier and have larger clutches as well as more often having second broods than first-years. In Scotland, females aged two or more years on average laid a week earlier than first-years, had a larger clutch (5.2 eggs versus 4.8 for first-years) and fledged more offspring both per brood (4.7 versus 3.8) and over the season (8.2 versus 5.1; Thompson 1992; and see Ward 1992). For pairs, the female’s age was more important than the male’s in determining laying date, clutch and brood size and number of fledglings. Pairs in which both members were old bred ten days earlier than pairs of first-years, and six days before mixed-age pairs; in the latter, where the females were older, laying was four days earlier than when they were first-years. Older females laid large clutches and first-years smaller ones whether they had older or first-year mates. Old pairs fledged more offspring (4.7) from their first broods than first-years (3.4), while older females with first-year mates fledged more (4.8) than first-year females with older males (4.5). One reason why older females have more eggs and fledglings is that they lay early (Thompson 1992) and date of laying, clutch and brood sizes, and the likelihood of having a second brood are related. For females recorded laying in successive seasons, first-years laid significantly later than in their second year, but there was no significant change for older females and no change in clutch and brood sizes. Other studies have found similar effects of age (e.g. Shields & Crook 1987; Loske 1994; Brombach 2004). In Denmark, females two or more years old also arrive and start laying earlier than first-years and have more fledglings (6.6 versus 5.1, Møller & Szép 2005a). The difference in breeding performance between old and young females, however, was less in years with warm springs, presumably when feeding conditions made it easier for all birds to rear offspring. Individuals followed over successive years had an average first-brood size of 3.8 as first-years and 4.0 the following year, with respective second-brood sizes of 4.0 and 4.1 and this increase between years was

14639.qxd

24/1/06

154

3:53 pm

Page 154

The Barn Swallow

Figure 9.1 Fledgling production of Barn Swallows varies with age, being highest for three-year-olds. Vertical lines represent standard errors. From Møller & de Lope 1999.

higher after a high (and thus mild) North Atlantic Oscillation winter (Chapter 10; Møller 2002c). Males also fledge more young as they get older. Those two or more years old in Scotland had partners who laid early and reared more fledglings (4.6 per brood, 7.8 over the season) than first-years (3.5 per brood, 4.7 over the season; Thompson 1992). In Denmark, older males reared 7.1 fledglings over the season versus 5.7 for first-years (Møller & Szép 2005a). Senescence, however, eventually takes over. Møller & de Lope (1999) found that the number of fledglings per year increased up to age three years, then decreased (Figure 9.1). Old individuals, especially those five or more years old, have more asymmetric wings and tail suggesting that they are in poorer condition; in Møller & de Lope’s study they also had more parasites and arrived later in the spring: three to four-year-olds had the fewest mites in their nests and three-year-olds the fewest lice on their feathers. The reproductive performance of older Barn Swallows will be affected by the larger numbers of parasites, late arrival and possibly reduced foraging efficiency related to their wing and tail asymmetry. Although second-year birds may lay early and have time for more broods, some aspects of breeding performance start to deteriorate with age after the first breeding season. Both male and female Barn Swallows have smaller chicks, with slower feather growth, as they get older; the immune response of the chicks also weakens as the age of their mother increases (Saino et al. 2002f; Chapter 8). Although the chicks’ weights were similar in the first two breeding seasons, these then also declined with the age of their fathers in the same study. The loss of condition with age is reflected in the birds’ health. Among Italian Barn Swallows aged one to six years (males) and one to four years (females), the

14639.qxd

24/1/06

3:53 pm

Page 155

Productivity and survival

155

primary immune response (to initial vaccination with Newcastle disease virus) was lower for older females and the secondary immune response (to vaccination the following year) was lower for both older males and females (Saino et al. 2003d). This finding suggests that reproduction is more costly for females than for males, possibly because of, for example, egg-laying, transferring nutrients to the egg, and feeding chicks more than males do (Chapters 7, 8; Saino et al. 2003d). Females that do reach an old age, though, differ in health as well as fecundity and arrival date from other females and tend to be those that have relatively small first clutches when a year old (A.P. Møller, F. de Lope & N. Saino, unpubl. data). Males and females tend to get larger with age, at least with respect to wing and tail length (Chapter 1). Reproductive success thus tends to increase with both age and size. Size alone seems to be of little importance, however, especially in females, whereas longer-tailed males breed early, are more likely to have two broods and produce more fledglings (Chapter 4). Skeletal measures of size are not generally related to reproductive success (Thompson 1992; Saino et al. 1997e). Individuals clearly differ in how many chicks they are able to fledge. Some pairs can end up with none or just one or two chicks in a season, whereas others can rear as many as 16 (e.g. de Lope Rebollo 1983). Thompson (1992) noted that, over three years, one female laid 39 eggs with a hatching rate of 49% (one to four eggs were infertile in each of seven attempts with two partners) and another hatched all 30 eggs in six clutches of five, also with two partners. Males vary even more in ability, some remaining unmated and others having offspring with both their social mates and other females (Chapter 5). The lifetime record is probably that of an 11-year-old male who had 101 fledglings with five females (Brombach 2004), although it is not known how many of these were the male’s own offspring, or how many additional ones he sired with extra-pair partners.

ENVIRONMENTAL FACTORS Habitat and the weather In Europe at least, dairy farms are a high-quality habitat. Thus Barn Swallows in Italy bred earlier on farms with cattle; however, large numbers of cattle were associated with low fledging success (Ambrosini et al. 2002a). Ambrosini et al. suggested that farms with many cattle recruit more young Barn Swallows which produce fewer fledglings than older ones, lowering the average fledging success for the farm. At Møller’s (2001b) Danish study site, several aspects of breeding performance were associated with the presence of dairy cattle. Møller compared Barn Swallows breeding on farms before and after the farms abandoned dairying. Unlike the Italian study, there was no effect of the presence of cattle on laying dates for first clutches, but when dairying ceased, the size of first clutches declined from an average of 4.9 to 4.7, the frequency of second clutches fell from 66% to 46%, and the average annual reproductive success fell from 7.4 to 6.5 fledglings (Table 9.1). In addition, chicks

14639.qxd

24/1/06

156

3:53 pm

Page 156

The Barn Swallow

were smaller (as measured by tarsus length), weighed less, and were in poorer condition (as measured by haematocrit and white blood cell levels and their immune response; Chapter 8). Survival of such chicks may be poorer and fewer may be recruited into the breeding population. The adults themselves, however, were similar in size and condition before and after cattle were lost, so dairy farms did not attract better-quality birds. However, in England, Evans (2001) found that breeding success was not influenced by habitat type, in mixed-farming environments dominated by different proportions of pasture land. In these situations, where variation in habitat quality is less marked, Barn Swallows breeding in poorer habitat may work harder than those in high-quality habitats to maintain fledgling numbers, although this may be at the expense of their own survival (Evans 2001). Fledgling production varies between years, in part depending on weather and food availability. Numerous studies have recorded poor breeding success in seasons with cold, wet weather, and sometimes also in very hot, dry weather. Brombach (2004) found that the average number of fledglings per pair varied from 5.3 in a cold, wet summer to 7.3 when the summer was sunny and warm. Møller (2002c) found that the sizes of first clutches, and their success (measured as the number of 12-day-old chicks divided by clutch size), relative to those of second broods, increased after high North Atlantic Oscillation (NAO) winters, that is, when feeding conditions early in the year were favourable. First broods were around 30% larger or smaller than second broods in high and low NAO years, respectively. Productivity also varies geographically, with fewer offspring per year at high than at low latitudes; thus pairs in Spain can rear more than nine chicks but those in Finland average less than five (Møller 2001c). In general, environmental conditions on the breeding grounds seem to have most effect on how early breeding starts, clutch size and the percentage of pairs having a second brood (Chapter 7). Hatching and fledging success are probably normally affected to only a small extent by food abundance and the weather, unless these are particularly adverse, either too dry and hot or too cold and wet. In New York State, Shields & Crook (1987) found that egg desertion during severe weather was one of the main reasons for a low hatching rate of 78%, the majority of first broods in 1985 were lost during protracted cold, wet weather (Hebblethwaite & Shields 1990), and in another recent study bad weather was partly to blame for poor breeding success (R.J. Safran, pers. comm.). In Germany, Loske (1994) also recorded low hatching success and high chick mortality in first broods in poor weather. Normally, not many chicks starve to death, however, and there is hardly any starvation in Italy or Spain (A.P. Møller, pers. comm.). In Møller’s (1988b) study 29% of chick deaths were attributed to starvation and in Scotland 16% (Thompson 1992). Møller (2001b), however, found no effect of the cessation of dairy farming, and Evans (2001) found only weak effects of the weather, on hatching and fledging. Saino et al. (2004b) also found no effect of ambient temperature during incubation on the hatchability of eggs. In contrast, the health and condition of the chicks, and hence probably their chance of survival, are affected by feeding conditions (Chapter 8). Environmental conditions in the winter quarters also influence productivity, by affecting the time of breeding and hence the number of fledglings produced (Saino et al. 2004c).

14639.qxd

24/1/06

3:53 pm

Page 157

Productivity and survival

157

Pesticides and pollution Pesticides and other pollutants can accumulate in the insect prey of Barn Swallows, and the birds can in turn accumulate enough of the substances to be affected themselves. The effects on breeding Barn Swallows vary but locally breeding success may suffer (Glutz von Blotzheim & Bauer 1985). Fossi et al. (1994), for example, recorded a decline over four years in the number of nests and in clutch size in cowsheds in Italy where an organophosphate insecticide was used to kill flies; after the insecticide application, Barn Swallows showed decreased blood levels of B-esterases, of sufficient magnitude to induce sublethal effects such as neurological disorders (Massi et al. 1991). High levels of polychlorinated biphenyls (PCBs) and other organochlorines, which are hormone disruptors, have been found in tissue samples of Barn Swallows in Italy (Kannan et al. 2002). The effect of such contaminants on Barn Swallows has not been studied but in another hirundine, the Tree Swallow, high concentrations of PCBs were associated with the building of small, poor-quality nests, females deserting and eggs failing to hatch; in addition, females developed adult coloration at a younger age and started breeding earlier (McCarty & Secord 1999a, b, 2000). It is likely that organochlorines would have similar effects on Barn Swallows. A more serious effect of the widespread use of pesticides, however, is a reduction in the Barn Swallow’s food supply. Even biological control agents, which are not toxic themselves, can deplete insect life enough to reduce breeding success of insectivorous birds. For example, after treatment of fields in Córdoba Province, Spain, with Bacillus thuringiensis, the local Barn Swallows hatched fewer eggs and had smaller second clutches (Cabello de Alba 2002). Other pollutants are also picked up from the environment. At Martin Lake in Texas in the 1980s, where the lake was contaminated with selenium, Barn Swallows had high levels of selenium in their kidneys and in their eggs, although nesting success did not seem to be affected (King et al. 1994). Barn Swallows nesting along a highway in Maryland contained larger concentrations of lead than those from a rural area, although again breeding success was unaffected (Grue et al. 1984). Barn Swallow feathers have been found to contain heavy metals as well as organochlorine pesticides (Gavrilov et al. 1994). Radionuclides are also known to accumulate in Barn Swallows nesting near radioactive sources; at high enough doses, such as those from the nuclear accident at Chernobyl in 1986, these may affect chick growth and survival and impair the adults’ feather growth and immune function (e.g. Millard et al. 1990; Møller 1993b; Camplani et al. 1999).

NEST COMPETITORS AND BROOD PARASITES Barn Swallows do not have many serious competitors for nest sites or nests. Other mud-nest-building hirundines, such as Northern House Martins, Red-rumped

14639.qxd

24/1/06

158

3:53 pm

Page 158

The Barn Swallow

Swallows and Cliff Swallows, prefer more outdoor sites and nest below horizontal surfaces rather than on beams and ledges. These species have enclosed nests, which are thus less exposed to predators and the weather than an open Barn Swallow’s nest would be. Thus, where they nest together, Barn Swallows tend to nest further inside barns and Cliff Swallows near the entrance or outside (e.g. Samuel 1971b). However, it is not clear whether Barn Swallows are sometimes prevented from nesting in outside places by such competitors. Cliff Swallows are dominant to Barn Swallows at nest sites and may put them off nesting in certain places (Brown & Brown 1996, 1999a). In contrast, Mizuta (1963) suggested that Barn Swallows in Japan were dominant to Red-rumped Swallows. Several species, such as Eastern and Say’s Phoebes, Northern House Martins, Cliff Swallows, Cave Swallows, House Sparrows, Eurasian Tree Sparrows, Black Redstarts, House Wrens, Winter Wrens, European Robins, Spotted Flycatchers and bats will take over Barn Swallows’ nests for their own, or as supports for their own nests, but they usually use old, unoccupied ones (e.g. Samuel 1971b; Vansteenwegen 1982; Brown & Brown 1999a). Barn Swallows can be very aggressive and will sometimes drive other birds such as Northern House Martins and Red-rumped Swallows away from these species’ nests, even destroying the latter (e.g. Mizuta 1963; Coan 1990). However, they are also sometimes evicted by other species, especially European Starlings and House Sparrows (e.g. Boyd 1935, 1936; Jarry 1980; Vansteenwegen 1982), but also other hirundines such as Tree Swallows and Northern House Martins (e.g. Radermacher 1970; Butler & Campbell 1987; Andrew 1993). In one case, however, a pair of Barn Swallows and a pair of Say’s Phoebes laid in the same nest and incubated and brought up the chicks together, although their interactions were not amicable, and successfully fledged two of each species (Kozma & Mathews 1995). House Sparrows can be a particular problem, as they will destroy eggs and chicks as well as take over nests, and were even blamed for the complete loss of Barn Swallows in parts of New England in the 1800s and for declines elsewhere (Kingery 1998; Brown & Brown 1999a). Weisheit & Creighton (1989) recorded them stealing feathers and pecking and removing young chicks from the nest. They also had circumstantial evidence of their pecking at and removing eggs. In this study 25% of the eggs laid failed to produce fledged young because of known or suspected House Sparrow damage. Other studies, particularly in North America, have also blamed House Sparrows, at least in part, for low breeding success, especially hatching success (e.g. Anthony & Ely 1976; Jarry 1980; R.J. Safran, pers. comm.). Why House Sparrows behave in this way, however, is not known; they do not always seem to benefit by acquiring a nest. Barn Swallows rarely suffer from avian brood parasites. Cases of Common Cuckoos laying in their nests in Britain are rare (e.g. Young 1974; Bowden 2005; Pankhurst 2005), as are cases in North America of Brown-headed Cowbirds parasitising Barn Swallows (Wolfe 1994).

14639.qxd

24/1/06

3:53 pm

Page 159

Productivity and survival

159

PARASITES Barn Swallows suffer from many parasites, both blood-suckers in the nest and plumage and internal parasites (Møller 1994a; Brown & Brown 1999a). Møller (1994a) recorded 12 species at his Danish site and others occur elsewhere. The more common ones include the tropical fowl mite, feather lice, louse flies, blow flies and the swallow flea. The types of parasites and the infestation level vary between sites and years. Fowl mites were the most important parasite at Møller’s Danish study site in the 1980s but had little effect in the 1990s, and in Spain martin bugs were common in one year of a two-year study and the latter site had greater numbers of parasites (de Lope & Møller 1993a). A blood parasite Haemoproteus prognei has been recorded in a quarter of Barn Swallows in Spain, increasing in intensity and prevalence in older birds, but is rare in Denmark and Italy (Møller et al. 2004b; A. Marzal & F. de Lope, unpubl. data). Blow fly larvae can be common in Barn Swallow nests in Britain (Owen 1955); and in New York State, these were the main parasite (Shields & Crook 1987). Other animals also found in the nests include book-lice and beetles which feed on dead animal matter, hemipteran bugs and pseudoscorpions which prey on mites, chalcid wasps which lay their eggs in the fly larvae present, and moth larvae which feed on feathers (e.g. Boyd 1935; Brown & Brown 1999a). One of the best-studied parasites of Barn Swallows is the tropical fowl mite, which feeds on the birds’ blood and is known to have several detrimental effects (e.g. Møller 1990a, 1991a, 1993a). Some mites overwinter in the nests waiting for the birds to return and their numbers quickly build up once breeding starts. While many nests may remain relatively free of mites, a few can contain 10,000 or more. Parents carrying mites seem to be the main source of mites in nests. About a third of adults arriving at Møller’s breeding site in the 1980s, for example, already had mites on them. When Møller (1990a) added mites to first-clutch nests there was no significant effect on first-brood chicks, but fewer chicks fledged from the parents’ second-brood nests than when mites had been removed (an average of 3.6 chicks versus 4.3). In addition, the survival of fledglings in their first week was impaired: the average number surviving to independence from first-brood nests with added mites was only 2.8 and from the parents’ second-brood nests only 2.3, compared to 3.8 and 3.3 fledglings, respectively, from first- and second-brood nests with no mites added. Pairs whose nests had had mites added produced an average of 4.3 offspring over the season, whereas those with mite-free nests reared 6.4 and non-manipulated pairs reared 6.2 fledglings. For mite-added nests, 53% of eggs produced fledglings, whereas 73% did so for mite-free nests. Møller (1990a) also found a reduction in hatching success in second clutches from 98% for pairs with nests from which he removed all mites to 95% with nonmanipulated nests and 91% with nests with mites added. An experiment involving manipulation of clutch sizes and parasite levels (Møller 1993a) showed that, as well as having a direct effect on second broods, mites could affect them indirectly by increasing the costs of rearing first broods and reducing the parents’ ability to rear

14639.qxd

24/1/06

160

3:53 pm

Page 160

The Barn Swallow

second ones. Møller (1993a) changed first-clutch sizes by adding or removing an egg, and mite levels by spraying some nests to remove the parasites and leaving others with mites. Changing the clutch size broke the relationship with female quality, that is, that good-quality females can rear large broods more easily than poorquality females. The presence of mites interacted with the costs of rearing a clutch. Thus, females that had an enlarged clutch and mites in the nest were less likely to have a second clutch; if they did have one, they delayed laying it, and had smaller clutches and broods at fledging and lighter chicks. The effort of breeding may itself make the parents more susceptible to infection, perhaps by impairing the efficiency of the immune system: pairs with larger first clutches had more mites in their nests if they did start a second one (Møller 1993a, 1997), and parents with large broods are likely to be exposed to large numbers of parasites (Saino et al. 2002g). The effect of the mites declined over time, however. Møller repeated his experimental addition and removal of mites in 1999 when the population appeared to have developed resistance to the mites and the parasites were less abundant, and this time the proportion of eggs producing fledglings was similar for the two types of nest: 76% for nests with mites added and 75% for mite-free nests (Møller 2002b). The chicks appeared to be more resistant to the mites that were present. Breeding success was negatively correlated with the prevalence of mites in this population (Møller 2002b; Figure 9.2) Parasites can affect the health of the chicks directly and also limit growth by forcing the chicks to allocate resources to their immune systems instead. In some cases, the parasites compromise the growth of the chicks (e.g. Saino et al. 1998); in others their effect is more severe, leading to chicks dying, perhaps directly from loss of blood or from the combined effects of parasites and food shortages (e.g. Shields & Crook 1987; Barclay 1988). A lack of food may depress the chicks’ immune systems, so that they are unable to resist the attacks of parasites (Merino et al. 2000). Chicks

Figure 9.2. Reproductive success (fledglings produced as a percentage of eggs laid) of Barn Swallows decreases with increasing prevalence of mites. From Møller 2002b.

14639.qxd

24/1/06

3:53 pm

Page 161

Productivity and survival

161

with a good immune response are more likely to survive (Merino et al. 2000; Saino et al. 2003e). In one study, parasites were the main cause of a high rate of nest failure, killing 32% of chicks, although bad weather probably contributed to this mortality (Shields & Crook 1987). Second broods were most affected: only 26% of parasitised nests produced at least one fledgling and the average was only 0.7 fledglings, whereas 83% of unparasitised nests had at least one fledgling, with an average of 3.5 fledglings. Parasites affected first broods to a lesser extent, probably because parasite infestations were lower early in the season. In contrast, Møller et al. (2001) found that chick mortality caused by parasites was only 4.4% and Saino et al. (1998) found that louse flies had no effect on chicks, with very few dying of any cause. There can also be subtle effects of parasites on the cost of breeding (Møller 1993a, 1994a). By affecting a bird’s health, they may make it more susceptible to other costs. For example, an incubating female infested with parasites may need to forage for longer and so may expose the clutch to infanticidal conspecifics and predators; Saino et al. (1998a) suggested this as the reason for losses of eggs in nests heavily infested with louse flies.

OTHER EGG AND CHICK LOSSES A small percentage of eggs are infertile or fail to hatch because the embryo dies. Other reasons for egg losses include parents dying or deserting, nest falls, damage by nest competitors, or eggs being tossed out or falling out, but these are usually infrequent. For newly hatched chicks, infanticide can be a serious cause of mortality. Møller (2004a) noted that its importance varied over a 25-year period from insignificant when the population was small to more than 25% of chick mortality at high densities (averaging 1.8%). Crook & Shields (1985) found that it accounted for 16% of chick mortality over five years. Infanticide has not been observed in all studies, however (e.g. Myers & Waller 1977; Medvin et al. 1987; Thompson 1992). Predation is also rare, usually causing less than 10% of losses (e.g. Ribault 1983; Crook & Shields 1985; Møller 1987d; Lorek 1992; Brichetti & Caffi 1992; Thompson 1992). House Sparrows, rats, cats and humans are often cited as the main predators. Nests are vulnerable to rats and mice, which are known to take eggs, chicks and sitting adults. Other nest predators include owls, corvids, grackles, squirrels, Eastern Chipmunks, Garden Dormice, Weasels, Raccoons, Bobcats, dogs, snakes and ants. As well as taking down nests in what they consider to be unsuitable sites, people also often cause disturbance, which can make parents desert. Disturbance accounted for 14% of chick losses in Scotland (Thompson 1992). Although usually minor, predation can be locally important. Alatalo (1976) blamed predation, mostly by Common Magpies, as the main reason for the low breeding success in his study (Table 9.1). In one case a Bobcat destroyed 34 nests at a single site (Lohoefener 1977); fire ants consumed eggs or young in 25% of nesting

14639.qxd

24/1/06

3:53 pm

Page 162

162

The Barn Swallow

attempts in a Texan culvert (Kopachena et al. 2000); Jarry (1980) attributed 20% of nest failures over seven years to dormice; and Carrion and Large-billed Crows destroyed 12% of nests in Hiroshima (Suzuki 1998). Other factors such as chicks falling out of nests, nest falls and heat stroke are generally not important causes of chick mortality, accounting for only a few per cent of losses, but they may at times have severe effects. The sites used for nests may sometimes get very hot during sunny weather, for example, especially if the nest is close to a wood or metal roof, and chicks can die as a result (e.g. Mason 1953; Anthony & Ely 1976; F. de Lope, pers. comm.; M. Thompson, pers. comm.). Both clutches and broods are sometimes abandoned; this may be the result of a variety of factors such as bad weather, partial nest predation, a parent dying, or disturbance, although the cause is often not clear.

SURVIVAL The extensive long-term ringing of Barn Swallows, and subsequent recoveries of ringed birds, has allowed reasonable estimates to be made of annual survival rates (the probability of an individual surviving from one year to the next for large populations). Return rates of birds to study sites have also been used as estimates of survival rates. These are more problematic because they assume that birds that do not return have died, rather than moved elsewhere, because of poor breeding success, for example. This assumption is probably robust for adult Barn Swallows, because few adults move away from the sites where they first bred (Chapter 10). Nevertheless, small study areas may miss the few birds, especially females, that do change sites between years, and long-term, large-scale studies are more likely to pick up movements from the previous site and hence produce return rates that reflect true survival rates. Return rates of juveniles do not reflect survival rates, because juveniles tend to disperse from the natal sites (Chapter 10).

Juveniles At least for their first few weeks when they are learning to feed themselves, fledglings are very vulnerable, especially to predation. One factor that may influence their chances of survival is their peak or later chick weight and factors that reduce their weight may also affect their survival. In their first week out of the nest, fledglings survive less well if they come from mite-infested nests than from mite-free nests, probably because of their lower weight: Møller (1990a) reported that fledgling survival from first broods was 90.1% for mite-free nests, but only 64.9% for mite-infested nests, and from second broods 78.3% versus 63.8%. Survival to the first breeding season, and hence recruitment into the breeding population, may also depend on the condition of the bird as a chick and recent fledgling. Results are meagre, as the recruitment rate to the natal area is low anyway and

14639.qxd

24/1/06

3:54 pm

Productivity and survival

Page 163

163

many recruits may not be found, but they suggest that chick weights and date of hatching are important factors. The earlier in the season a young Barn Swallow hatches and fledges, the better the conditions are likely to be in terms of food supply or daylength available for feeding. Second broods in particular are likely to benefit from hatching early. In Scotland, of 1,600 ringed fledglings 49 were caught as adults, 47 in the study area (Thompson 1992). The majority of these were from first broods (27 first, 15 second, 5 unknown) and hatched at peak hatching periods, the earliest being 22 May and 1 June, but the latest did not hatch until mid-August. This proportion varied between years, with nearly all coming from first broods in one year but only half in another. Four pairs each produced two recruits from their first brood or both first and second broods. The recruits tended to be heavier as chicks than non-recruits and to be the heaviest and largest, in terms of wing length, in their brood. There was no clear relation with brood size; the number of recruits increased with brood size in one year, but broods of six produced only two. The age of the parents and whether they had one or two broods also did not seem to affect whether their offspring returned. There were few recruits from broods that had been artificially enlarged or reduced, particularly from broods of eight, suggesting that parents are more likely to produce recruits from their natural clutch size. Brombach (2004) also found that first broods produced more recruits than second broods and that a higher percentage of young in broods of five became recruits (9.4%) than in other brood sizes (3.3–5.0%). Møller found that Barn Swallows that recruited to his breeding population weighed more as 15-day-olds than those that did not and were more likely to have hatched early in the season, from first broods, regardless of their weights as chicks (Møller 1991c, 1994a,f; Figure 9.3). Over the period 1984–2000 there were more recruits when fledglings from first broods made up a large proportion of the total number of fledglings of that year, confirming the importance of hatching early (Møller 2002c). Chick quality, in terms of immune function, for example, is also likely to be important, as this is related to the probability of survival (Merino et al. 2000; Saino et al. 2003e).

Adults Size has an effect on survival. Long-tailed males have a better chance of surviving to the next breeding season than short-tailed ones and are less likely to fall prey to Eurasian Sparrowhawks (Møller 1994a; Møller & Nielsen 1997; Saino et al. 1999b; Chapter 4), and Thompson (1992) found that surviving males were heavier with thicker breast muscles (i.e. greater protein reserves) than males that died. Female survival is related to weight and tail length, reflecting body condition (Brown & Brown 1999b; Møller & Szép 2002). Viability does not just depend on body condition in terms of fat and protein reserves, but also on other aspects of health such as immunocompetence. Males with a good immune response survive better than those with a poor one (Saino et al. 1997b). A good immune response may be particularly important for long-distance migrants, such as Barn Swallows, because of the strenuous

14639.qxd

24/1/06

164

3:54 pm

Page 164

The Barn Swallow

Figure 9.3. Early-hatched Barn Swallows are more likely to recruit into the breeding population. First (a) and second (b) broods. Numbers are numbers of chicks that fledged in a specific ten-day period. Dates are days since 30 April. From Møller 1994f.

migration itself and because they are likely to encounter pathogens in their winter quarters to which they have not been exposed before (Møller 2001c). Survival potentially depends on the effort put into rearing chicks, especially, for females, the number of broods reared in a season. When first broods were experimentally increased or decreased in size by one chick, Saino et al. (1999b) found that males were less likely to survive if they had had an enlarged brood and their offspring had high immunocompetence, and females were less likely to survive if they had large offspring (measured by tarsus length) also with high immunocompetence (Figure 9.4). Investing in current offspring may thus impair the survival of the parents. Saino et al. (1999b) suggested that the parents may allocate resources, such as proteins or carotenoids, to improve the immunocompetence of their offspring at their own expense, and, in the case of females, to improve offspring size as well. Females in this study were affected by an increase in brood size only when they had two broods rather than one. Having two broods reduced female survival when the first brood was enlarged. Rearing an enlarged brood thus impaired the survival of

14639.qxd

24/1/06

3:54 pm

Productivity and survival

Page 165

165

Figure 9.4. The probability of survival of male (a) and female (b) Barn Swallows is lower when their offspring have high immunocompetence, indicating a high level of investment by the parents. Closed symbols: broods experimentally increased by one chick; open symbols: broods reduced by one chick. From Saino et al. 1999b.

both sexes, whereas female survival was also impaired by having a second brood. In a similar experiment, Thompson (1992) found significant improvements in survival for double-brooded females rearing reduced second broods. However, experiments that force birds to rear a brood of a certain size can only reveal potential costs of reproduction. In reality, good-quality parents may be able to

14639.qxd

24/1/06

166

3:54 pm

Page 166

The Barn Swallow

care for a large brood with only minimal costs to themselves, whereas poor-quality parents may reduce their survival if they tried to rear a brood of the same size. Møller & Szép (2002) analysed the long-term survival rates of unmanipulated Barn Swallows in Denmark and there was no effect of number of offspring reared in a year or of the frequency of second broods on survival rates. Based on individuals returning to breed, Møller & de Lope (1999) found that survival rates increased from one to two-year-olds and decreased for individuals of five or more years of age. Males and females also differ slightly in survival rates, but the extent of the difference is generally small and varies between studies and years. For British Barn Swallows, there seems to be no marked difference in survival rates, calculated from national ringing data. Between 1966 and 1978, for females the estimated survival was 40%, marginally better than for males at 37%; this small difference may be caused by the inclusion of young birds, as sex differences may be more apparent in older individuals (Dobson 1987). Over a longer period, 1962–1995, survival rates during a period of increasing population were 37.2% for adult males, 33.7% for adult females, 61.2% for first-year males and 57.6% for first-year females, whereas when the population was declining the survival rates were similar for adults (36.8% for males, 33.4% for females), but lower for first-years (35.4% for males and 32.0% for females); there was no significant effect of sex, however, and only a marginal effect of age (Siriwardena et al. 1998a). In Scotland, adult survival rates from 1987 to 1988, calculated as recapture rates, were 48.6–57.1% (minimum and maximum estimates) for males and 42.9–56.3% for females, but were 32.5–41.4% and 24.9–32.3%, respectively, in the following year when the population size was lower; survival was higher for first-years (57%) than older birds (48%) (Thompson 1992). In Nebraska, males and females also had similar survival rates, averaging 35.0% over a 15-year period (Table 9.2). In contrast, in Møller’s Danish population, which has been declining over the last three decades, the survival rates of adult males and females during 1984–1993 were significantly different, and very low, at 28.4% and 25.5%, respectively (Møller 1994). However, in a later analysis of the period 1984–1998, male survival was higher at 34.3%, not significantly different from that of females at 33.8%, although female survival rates were more variable (Møller & Szép 2002). Male and female survival rates did not co-vary, indicating different causes of mortality for the two sexes. The survival rates for this population are not high enough to prevent it from going extinct in only about 20 years (Møller & Szép 2002). The latest analysis of this population indicates a particularly low survival rate for yearling females and an Italian study also found low survival rates for females (Table 9.2). There is often an excess of males in the breeding season (Chapter 5), which suggests that females suffer higher mortality than males, although the survival rates given above differ only slightly. In Denmark, the percentage of unmated males increased in years after high mortality in the winter (Møller 1994a). This finding, the more variable survival rate of females and the low survival rate of young Danish females may suggest that females fare worse than males when environmental conditions are poor. Possibly, females are more stressed by reproductive activities, especially in their first breeding

14639.qxd

24/1/06

3:54 pm

Page 167

Productivity and survival Table 9.2.

167

Examples of survival rates of Barn Swallows.

Locality

Survival rate (%)

Period (number of birds)

Source

Britain

1983–2001 (350)

Britain

81.1 (for fledglings up to 45 days after hatching) 56.7 (remainder of juveniles) 39.8 (adults)

1983–2001 (91)

Denmark

30.9 (yearling males)

1984–2003 (18)

Denmark

23.5 (yearling females)

1984–2003 (18)

Denmark

35.6 (older males)

1984–2003 (18)

Denmark

37.2 (older females)

1984–2003 (18)

Germany Italy Italy Kazakhstan Nebraska, USA

33.0 37 (males) 26 (females) 49.5* 35

1959–1968 (238) 1988–1996 (364) 1988–1996 (504) 1966–1979 (56) 15 years (300)

BTO national ringing data BTO national ringing data BTO national ringing data Møller & Szép 2005a Møller & Szép 2005a Møller & Szép 2005a Møller & Szép 2005a Brombach 2004 Ferro & Boano 1998 Ferro & Boano 1998 Gavrilov et al. 2002 Brown & Brown 1999a

Britain

1983–2001 (442)

*Estimated for migrating birds.

year, and so are less able to survive periods of scarce food then or later in the winter quarters. However, males seem to be more susceptible than females to poor feeding conditions on migration in North Africa, perhaps because they make the migration faster, arriving a few days before females at the breeding grounds (Møller & Szép 2005b). They are also more likely to be taken by predators: in one study 71% of adult Barn Swallows killed by Eurasian Sparrowhawks were males (Møller & Nielsen 1997). In addition, sex ratios in Italian Barn Swallows suggest that excess female mortality occurs mainly between fledging and the following breeding season, rather than after the stress of rearing chicks: over nine years the proportion of males among chicks 7–12 days old was 0.492 whereas among yearlings it was higher at 0.544 (Saino et al. 2003h). Life expectancy for adults is only just over a year. In the British population, Dobson (1987) calculated it to be 1.68 years for females and 1.59 years for males. Typically only a few individuals reach six or more years. Saino et al. (2003d) recorded males living up to seven years and females five years, and Møller (pers. comm.) recorded only one seven-year-old out of 3,365 birds ringed as presumed first-years. The oldest Scottish Barn Swallow was nine years, the oldest North American Barn Swallow was eight years ten months, and there are records of birds reaching 11 years (Maute 2003; Brombach 2004; BTO ringing data). There are

14639.qxd

24/1/06

168

3:54 pm

Page 168

The Barn Swallow

also dubious records of 15- to 16-year-old birds (Glutz von Blotzheim & Bauer 1985; Cramp 1988); given the low survival rates, however, the chances of a Barn Swallow reaching such an age are slim.

JUVENILE AND ADULT MORTALITY Recent fledglings are at risk from predators, particularly if they have fledged at an early age. Crook & Shields (1987), for example, reported that, of ten fledglings killed or found dead, seven were taken by predators; all were less than five days out of the nest and two had left the nest at only 18 and 19 days. Newly fledged Barn Swallows are at risk from cats, in particular, and raptors such as Eurasian Sparrowhawks. Opdam (1979) found that Barn Swallows formed only 1.3% of the diet of Eurasian Sparrowhawks overall, but of those taken in June 29% were juveniles, and in July 47%. Youngsters also seem to be poor at avoiding traffic; in one British study of Barn Swallows found dead, and for which the cause of death was known, 40% of recent fledglings were road casualties, in contrast to 13% of those found over the next 11 months of life, and 8% for older Barn Swallows (Mead 2002). Young Barn Swallows are frequent road casualties in Eastern Europe, perhaps reflecting the high densities of breeding pairs there (Chapter 3; Erritzoe et al. 2003). Eurasian Hobbies take many Barn Swallows; in a study in central Europe, they formed 30% of the bird prey taken, although birds comprise only part of the diet (Cramp 1980). Other avian predators of juvenile and adult Barn Swallows during the breeding season include Parasitic Jaegers, California Gulls, Great-tailed, Common and Boat-tailed Grackles, Northern Goshawks, American Kestrels, Merlins and Tawny and Barn Owls. Eleonora’s Falcons take migrant hirundines in the Mediterranean, although relatively few Barn Swallows. In the non-breeding season, Barn Swallows face a different array of predators, some of which may be attracted to the often large roosts. These include numerous raptor species such as Gabar and Red-chested Goshawks, African and Eurasian Hobbies, Grey Kestrels, Yellow-billed Kites, Red-necked and Lanner Falcons, Peregrines and Barn Owls (van den Brink et al. 1997, 1998, 2003; Bijlsma & van den Brink, in press). Predators are likely to take only a very small proportion of Barn Swallows, however. At a roost of 1.5 million Barn Swallows in Nigeria, for example, the main bird predator, the African Hobby, took up to 14 birds a day, and over the whole season raptors probably took only about 5,000 birds (Bijlsma & van den Brink, in press). Adult mortality is low during the breeding season and only the occasional bird is taken by a predator, often a rat, cat, owl, or hawk. More unusual predators include fish and Bullfrogs. Severe weather in the breeding season may also cause, or contribute to, some deaths (Crook & Shields 1987; Thompson 1992; Brown & Brown 1999b). A few adults, as well as juveniles, especially those that nest on highway bridges and culverts, collide with buildings or cars, and some have become entangled in fishing line or horsehair used as nesting material and in vegetation (e.g. Dobson

14639.qxd

24/1/06

3:54 pm

Productivity and survival

Page 169

169

1987; Burton 1994; Brown & Brown 1999a). In Britain, about 70% of reported deaths are human-related, such as traffic accidents or birds being trapped inside buildings (sash windows are a particular problem), and 11% are due to domestic predators, mostly cats (Mead 2002), although of course these reflect the situations where people are likely to find a dead bird and not the main causes in the population as a whole. In Dobson’s study of survival rates in the British population, about half the birds were found dead; about 14% of both sexes had hit a building, more males than females (8% and 5%, respectively) were hit by a car or train and 8% of males and 3% of females were taken by cats. Occasionally there are incidents of Barn Swallows dying directly from pesticide poisoning; for example, about a hundred were found dead in the department of Yonne in France in May 2004 with high concentrations of Fipronil and Imidaclopride (Ligue pour la Protection des Oiseaux 2004). People are also sometimes predators of Barn Swallows. Barn Swallow feathers were used in the millinery trade in the 1800s. Concern over this killing indirectly led to the creation of the first Audubon Society and hence to the conservation movement in the USA (Brown & Brown 1999a). The impact of this hunting is unknown, however. Barn Swallows are one of many species shot at or trapped by hunters, some for the pot or for sale, or just for target practice. Shooting used to be particularly serious in Malta, with at one time an estimated 160,000–430,000 hirundines shot annually there (Fenech 1992). The European Union’s Bird Directive nowadays does not permit hunting of breeding birds or of migrants passing through to the breeding grounds; some illegal hunting continues, but this is likely to have a minor effect on numbers of Barn Swallows (RSPB 2004). Hirundines at winter roosts or on migration are sometimes trapped for food. Some 12% of recoveries of British and Irish Barn Swallows and 9% from Spain are deliberately caught, mainly while on migration in Africa (Mead 2002; A.P. Møller, pers. comm.). For example, in the Ebbaken-Boje area of Nigeria, used by about 40 million Barn Swallows over the winter, local people used to take large numbers, catching them with glue spread on palm twigs (Micheloni 2003). In 1995 alone, one village caught about 200,000 Barn Swallows, which formed an important source of protein. Since 1995 a campaign to stop the hunting, and to provide the villagers with alternative sources of food, has helped to protect the birds (Loske 1996, 1999). In Xiangkhouang Province, in northern Laos, trappers use decoys with clap-nets and liming to catch migratory hirundines, including Barn Swallows, for food or for sale in local markets (Evans et al. 2000). Evans et al. estimated that more than 100,000 birds might be caught annually. Whether this is sustainable is not known, though large numbers were also being caught 60 years ago. In Thailand, Barn Swallows used to roost in hundreds of thousands at Bung Boraphet lake, but mass trapping for sale as food in local markets, together with destruction of reedbeds for lotus cultivation, has drastically reduced numbers; however, it is not clear how much this reflects a decline in population and how much a shift in roost site to sugar cane plantations (BirdLife International 2000). Migrating Barn Swallows are at risk from the vagaries of the weather, and torrential rain or spells of cold, wet weather, in which insects become scarce, have been

14639.qxd

24/1/06

170

3:54 pm

Page 170

The Barn Swallow

responsible for many deaths. Bad weather has caused mass mortalities several times in the past century, for example in the autumns of 1931, 1936 and 1974 in central Europe when hundreds of thousands of migrating birds perished (Ruge 1974; Glutz von Blotzheim & Bauer 1985; Chapter 10). On the wintering grounds, too, the weather may turn bad and several instances of mass deaths have been recorded (e.g. Broekhuysen 1953; Skead & Skead 1970). Although Barn Swallows will delay returning to their breeding grounds if the weather in the early spring is bad, breeding birds, particularly those arriving early, are still at risk if the rain and cold persist into the late spring, or return after a fine spell. In 1982 in the Sacramento Valley, California, for example, over a hundred Barn Swallows and other hirundines died in a long period of low temperatures and heavy rain (DuBowy & Moore 1985). In Utah in late April and May 1975 cold weather with snowfalls killed many migrants; post-mortems showed that the hirundines had very low fat levels and atrophied muscles (Whitmore et al. 1977). Møller (1994f ) and Brown & Brown (1999b) also noted mortality of Barn Swallows related to cold spring weather. During cold spells, Barn Swallows will try to minimise energy loss by roosting in warmer, or more sheltered, places such as buildings and by huddling together, perching closer to other birds, of their own or of other species, than they normally would; they will also cluster together in nests, either their own or of conspecifics or other species. For example, in late May 1967 in the Volga-Kama Reserve, southern Russia, when the temperature dropped to 4 °C, hundreds of Barn Swallows sheltered in a building and in nestboxes, and many were later found dead (Ayupov & Tazetdinov 1977). Similarly, Ytreberg (1986) recorded five Barn Swallows huddling together in a barn on a cold day in June 1981, in Norway, and up to seven clustering in a nest, including the owners. The body temperature of starving birds will drop several degrees in severe conditions, thus saving energy (Lyuleeva 1973; McKechnie & Lovegrove 2002). This facultative hypothermia, caused by low external temperatures, is only very mild, however, and is not the same as the torpor of some other birds such as poorwills and hummingbirds which can lower their body temperature by more than 10 °C. Barn Swallows found in this condition inside houses, in crevices in rocks and cliffs or in tree holes and old nests during cold weather (e.g. McAtee 1947) may have contributed to the idea that they spent the winter in this condition (Chapter 10), but they would be able to survive only a few days at most and such individuals are often moribund and die. Most deaths occur outside the breeding season and are associated with adverse environmental conditions. Møller (1989a) found that winter mortality was related to the weather in March in South Africa, being highest when there was little rainfall. Dry weather tends to be associated with a scarcity of insect prey, which may have most impact when Barn Swallows are feeding up before migrating. If water levels are low, wetland roost sites may also be restricted, increasing both distances to foraging sites and competition among the birds (van den Brink et al. 2000). This has consequences for both body weights and the rate of moult. Wintering Barn Swallows increase their weights once the rains start. In Botswana in 1992/93–1994/95,

14639.qxd

24/1/06

3:54 pm

Productivity and survival

Page 171

171

for example, Barn Swallow weights were low during dry periods and increased after rainfall when flying termites became abundant, and Barn Swallows moulted fastest in seasons with plenty of rain and roosting habitat (van den Brink et al. 1997, 2000). Juveniles may be particularly affected: in Botswana, the proportion of juveniles at roosts decreased from about 70–80% to only 34% in a very dry year, suggesting either a high mortality or that they moved elsewhere. Just before migration, Barn Swallows may be particularly vulnerable because their moulting tail feathers may impair their hunting ability and those that do start on the return migration may have low energy reserves that make them more susceptible to adverse situations. Environmental conditions during migration may affect mortality more than those in the winter quarters. Szép & Møller (2005) found that survival of Danish birds is positively related to vegetation growth in Algeria (as measured by the ‘normalised difference vegetation index’, see Chapter 10), that is, to the feeding conditions that the Barn Swallows encounter after crossing the Sahara, but not to that in the winter quarters (Møller & Szép 2005b). Survival rates declined at the same time as conditions in Algeria deteriorated through the 1980s and 1990s. For British Barn Swallows, too, conditions on migration in spring may be important for survival, as the numbers of breeding birds are weakly related to rainfall in the Sahel region (especially on the northern edge) during April, although not to that in southern Africa over winter (Robinson et al. 2003).

14639.qxd

24/1/06

3:54 pm

Page 172

CHAPTER 10

Migration and dispersal I myself, on the twenty-ninth of last October, . . . saw four or five swallows hovering round and settling on the roof of the county hospital. Now is it likely that these poor little birds (which perhaps had not been hatched but a few weeks) should, at that late season of the year, and from so midland a county, attempt a voyage to Goree or Senegal, almost as far as the equator? I acquiesce entirely in your opinion – that, though most of the swallow kind may migrate, yet that some do stay behind and hide with us during the winter. Gilbert White, 1789

For centuries, Barn Swallows were thought to spend the winter in rock or tree crevices or in mud under water in a torpid state; but by the beginning of the nineteenth century, observations of Barn Swallows at sea, in the English Channel, off

14639.qxd

24/1/06

3:54 pm

Page 173

Migration and dispersal

173

West Africa and in the Mediterranean, supported the alternative view that they migrated (Forster 1817). Only in the twentieth century, however, have ringing studies shown us the true extent of the Barn Swallows’ travels. The first confirmation of the winter home of British Barn Swallows came when a female ringed in Staffordshire by James Masefield (the brother of the poet John Masefield) in May 1911 was found in Natal on 23 December 1912 (Mead 2002). Since then millions of Barn Swallows have been ringed in many countries.

WINTER QUARTERS The winter ranges are generally south of the breeding ones, with little overlap. Barn Swallows of the subspecies rustica winter in sub-Saharan Africa and the Indian subcontinent. Within Africa, the majority winter south of the equator, but some stay in western and central areas. Barn Swallows tend to migrate to different areas depending on where they bred, although different populations mix to some extent. Individuals from across Europe migrate to southern Africa, but birds breeding in eastern areas tend to winter on the eastern side and birds from western areas on the western side (Loske 1986; Cramp 1988). The east–west divide is more marked in Central Africa than in southern Africa, with western and central European birds wintering between 10 °W and 26 °E in the tropics and northern and eastern European birds wintering between 22 ° and 34°E and in southern Africa. Barn Swallows from as far east as Krasnoyarsk Territory, Siberia (56°N, 95°E), and as far south as the West Tien Shan winter in southern and East Africa (Gavrilov et al. 2002). Barn Swallows ringed in southern Africa have been recorded from west, central and eastern Europe, with over half recorded from between 25° and 59°E in the breeding range; in Botswana, Namibia and the northern Cape there is a preponderance of western European birds and, in KwaZulu-Natal, eastern European ones (Oatley 2000). Recoveries of Eurasian-ringed Barn Swallows in southern Africa have mainly been in the south-east, although they are most frequently seen in eastern areas, especially the north-east and also in KwaZulu-Natal (Earlé 1997; Oatley 2000). Barn Swallows from northern parts of Europe travel the furthest. Thus British and Irish Barn Swallows are recorded in South Africa, Botswana and Namibia and seem to predominate in the western Cape. Scandinavian ones also occur in south-west and southern Africa, whereas those from central and southern Europe winter in westcentral Africa. For example, Italian Barn Swallows are known to winter in Ghana, Nigeria and the Central African Republic and Spanish ones in the Ivory Coast, Ghana and Nigeria (Møller et al. 2003; Saino et al. 2004a). However, a particular wintering site can host Barn Swallows from several areas; thus birds from the Netherlands, Belgium, France, Germany and southern Europe are found in roosts in Ghana (van den Brink et al. 1998).

14639.qxd

24/1/06

174

3:54 pm

Page 174

The Barn Swallow

Analysis of feathers has also provided evidence of wintering areas. The nitrogen and carbon content of feathers, which differs according to the geographical location of moulting birds, suggests that breeding birds in Møller’s Danish population moult in more than one area in Africa and possibly that some hatched in different areas (Møller & Hobson 2004), and indeed one recent breeding recruit came from south-west Sweden 130 km away (A.P. Møller, pers. comm.). Some individuals of the subspecies rustica winter in Pakistan and India. Those breeding in the western hills and northern mountains of Pakistan move down to the Indus and Punjab plains for the winter (Roberts 1992). Barn Swallows wintering in the Indian subcontinent probably include those breeding in southern Kazakhstan, Kyrgyzstan and western China (Gavrilov et al. 2002). Egyptian Barn Swallows, savignii, are resident, although they will gather in flocks when not breeding. The Middle Eastern subspecies transitiva probably migrates short distances. In the northern part of the breeding range of this subspecies there are both residents and summer visitors, and it has been recorded further west in Egypt in winter (Shirihai 1996). There have also been records claimed for Tunisia and Sudan and, less reliably, from East Africa and Zambia (Cramp 1988; Keith et al. 1992). The Asian subspecies migrate to southern areas, from the Indian subcontinent (mainly gutturalis) and south-west China as far east as Japan, the Philippines, Indonesia, New Guinea, Australia and Micronesia (where migrants are common on Palau, uncommon in the Marianas and Carolines, and rare on the Marshall Islands). Barn Swallows from eastern Russia (Transbaikalia to Primorye), Korea and Laos are known to winter in the Philippines, Malaysia, Indonesia, Thailand, Singapore, Hong Kong and Taiwan. A few gutturalis reach western New Guinea and the northern coast of Australia, from Western Australia to south-east Queensland. Australia is a recent extension to the wintering range; although one was reported in the Torres Strait in 1860, the next, at Derby, was not recorded until 1960 and Barn Swallows are now regular migrants to this region (Schodde & Mason 1999). This subspecies has also been reported in small numbers in winter on the south-eastern side of Africa in Botswana, Zimbabwe, Transvaal, Natal and Mozambique but the validity of these reports has been questioned (Keith et al. 1992). It is likely that they are rustica originating from areas where rustica and gutturalis intergrade (Gavrilov et al. 2002). The subspecies tytleri winters irregularly from Bengal east through Bangladesh, Bhutan, Assam, Nagaland, Manipur, southern Yunnan, Myanmar, Thailand, Peninsular Malaysia and central Annam; saturata has been recorded in southern Japan and mandschurica in Thailand and Taiwan (Brazil 1991; Robson 2000). The North American subspecies winters mainly in South America (Brown & Brown 1999a). Only small numbers reach eastern Brazil or further south than central Chile and northern Argentina, and few go as far as Tierra del Fuego and the Falkland Islands. Some winter further north, in Mexico and throughout Central America; in Panama, they occur mainly on the Pacific side. There are also records from the Galápagos Islands. They are mainly transients on islands in the Caribbean,

14639.qxd

24/1/06

3:54 pm

Migration and dispersal

Page 175

175

although there are records there throughout the year and regularly in winter on Hispaniola, Puerto Rico and the Lesser Antilles (Keith et al. 2003). Barn Swallows are sometimes reported further north into their breeding range, in winter (e.g. Cramp 1988; Brown & Brown 1999a). They are regularly recorded, usually in small numbers, in south-west Spain and along the Tyrrhenian coast of Italy, in particular in Tuscany, Lazio, Sardinia and probably Sicily (J.J. Cuervo, pers. comm; A. Pilastro, pers. comm.) and there are winter records from North Africa, coastal Arabia and southern Iran. There are also local or altitudinal migrant or resident populations in Afghanistan, Pakistan, northern India, Nepal and south Yunnan east to Taiwan, and possibly in Bhutan, north-west and north-east Thailand, north Laos and Tonkin; Barn Swallows also winter on the southern islands of Japan. In North America, Barn Swallows regularly occur in winter in California and Arizona, the coast of the Gulf of Mexico and southern Florida. Some of the birds recorded over winter in, for example, southern Europe and southern USA may be stragglers; others may be individuals that migrated to non-breeding quarters earlier in the year: in southern Spain Barn Swallows start to leave in June/July and spring migrants return as early as December (Møller et al. 2003; A.P. Møller, pers. comm.). Whether individuals also overwinter and moult in these areas instead of migrating is not known. A few Barn Swallows are recorded quite far north in winter as stragglers. In Britain, some, perhaps from late broods, linger into November or even late December, if the weather is mild, particularly in southern areas, but also in Scotland (e.g. Lack 1986). In 2004, for example, one was recorded on 5 December in northeast England, and in 2000 one at St Andrews on 25 December. King & Penhallurick (1977) described three surviving in Cornwall until early January and one was seen in late February; these birds occasionally foraged on the beach, picking up invertebrates from seaweed or sand. Early in the year, however, supposedly wintering Barn Swallows may be birds already returning from their winter quarters; such records are mainly from southern and south-eastern Britain and Ireland, suggesting they are on passage (Lack 1986). Britain generally has mild winters and Barn Swallows may be able to stay later than in harsher climates, but they have been reported in winter elsewhere in December to February in Europe, in favourable weather (e.g. Bruderer 1979; Guerrieri et al. 1990; Yeatman-Berthelot 1991). Locally abundant sources of food may delay autumn migration. For example, in the Urals, Barn Swallows have usually left by the end of September, but in October and early November 2000 some stayed on, feeding at a warm sewage outflow where flies were still swarming, even when snow had fallen (Lyakhov & Gusev 2001). In North America too, Barn Swallows are sometimes recorded in the northern parts of their breeding range in the winter months, usually as far north as Massachusetts (Brown & Brown 1999a). However, since 2000 Barn Swallows have been seen unusually frequently in western North America in late winter, sometimes in large numbers, for example 51 on 1 January 2002 in Monterey (Roberson 2002), 20–30 on Iona Island, British Columbia, on 31 January 2003 and 14 on Reifel Island, British Columbia, on 18 January 2004 (Anon. 2005).

14639.qxd

24/1/06

3:54 pm

Page 176

176

The Barn Swallow

Individual Barn Swallows are generally faithful to their winter quarters and are often recaught at the same roost (e.g. Nuttall 2003). A survey of Barn Swallows ringed in southern Africa showed that nearly all returned to the same place (68 of 120 controls) or to within 100 km of it (48 of 120 controls and 27 of 60 recoveries) between seasons (Oatley 2000). Elsewhere, too, Barn Swallows return to the same winter sites (Kang 1971; Medway 1973). However, the wintering areas sometimes change. British and Irish Barn Swallows extended their wintering range, which was mainly in KwaZulu-Natal, Free State and the eastern Cape, to the south and west after 1961 (Mead 1970), perhaps because of a combination of drought in eastern South Africa and wet weather, which would have improved the supply of insects, in the Karoo (Rowan 1972). When not breeding, Barn Swallows can be found in a wide variety of habitats from sea level to usually about 3,000 m (e.g. Keith et al. 1992). In the winter quarters, they inhabit mainly grassland, woodland, forest clearings and forest edge, cultivated fields and pasture, and, especially, swampy areas and waterbodies; they are reported less often from semi-arid and arid areas (e.g. Earlé 1997). One study of habitat use looked at the ratios of carbon isotopes which differ in woody vegetation and arid grassland; this difference is reflected in the composition of insects that feed on the vegetation and in the feathers of birds that feed on the insects. The carbon isotope ratio of feathers of Swiss Barn Swallows suggested that they had been feeding in woody areas, typical of southern West Africa, where Swiss birds have been recovered. In contrast, English Barn Swallows appeared to have been feeding in grassy areas, as are found in southern Africa where English Barn Swallows winter (Evans et al. 2003b). Barn Swallows are very abundant in Africa during the northern winter, often being the most abundant hirundine. Given a population of 16–36 million breeding pairs in Europe (Chapter 11), 80–190 million Barn Swallows may enter Africa each autumn from this area alone, as well as many from Asia. In road counts over 12 years, for example, Barn Swallows formed 74–96% of all hirundines seen (Broekhuysen 1964).

TIMING OF MIGRATION Barn Swallows migrate from their breeding areas because, particularly at high latitudes, their food supply falls dramatically in the autumn, the weather deteriorates, preventing them foraging, and the days are too short for them to get enough food. They thus have to fly to areas where food is still available and the weather more clement. Conversely, in the spring and summer, food is more abundant in the breeding quarters than the winter ones, where insect populations can be more stable; in a comparison of Scottish and Malaysian insect faunas, for example, the abundance of insects in Malaysia reached neither the lows nor the highs of the temperate area (Waugh 1978; Hails 1983). The current migration pattern probably developed

14639.qxd

24/1/06

3:54 pm

Migration and dispersal

Page 177

177

15,000 years ago after the last Ice Age: Barn Swallow populations could then breed further north, but the scarce food in winter would have led to long migrations to better feeding areas. The autumn migration is an extended affair. Barn Swallows that rear a single brood may leave early, whereas those rearing two or three broods may not fledge the last of them until September or early October. Juvenile Barn Swallows in Europe and Asia thus start dispersing as early as July, but the main migration is in late August–September in northern areas, including Scotland, Scandinavia, northern Russia and the Urals, and September–early October further south; some birds wait until late October or November, with a few stragglers in December. In Japan, the migration is from September in the north to mid-November in the south. In North America too, migrants can be seen from July mostly to early or mid-October with a few late individuals in November or December, and peak migration in northern areas such as Alaska, Canada and the north-eastern USA is late August to early September. Barn Swallows begin to arrive in northern Africa in late July and early August and in considerable numbers from mid-September to late October. The main arrival in southern Africa is in late October or November, with a few in August or September and some as late as December (Earlé 1997). Many early arrivals are adults, whereas juveniles predominate by January (Broekhuysen & Brown 1963). In South America, the first migrants have been recorded in August in French Guiana, Colombia and Suriname, early September in Brazil and Paraguay and late September in Argentina (Brown & Brown 1999a). Barn Swallows are present in their wintering grounds mainly from September to April. In Africa some are recorded in August and May and a few stay on in June and July, especially in the south-western Cape (Earlé 1997). Elsewhere, non-breeding birds will also stay in their winter quarters in the northern summer (e.g. Paynter 1995; Robson 2000). The return to the breeding grounds in Europe starts with a few birds in late January and February, and those breeding in southern areas also return early. The main exodus is from late February/March and most Barn Swallows have left southern Africa by late April. The peak movement in North Africa and the Mediterranean is mid-March to late April and in north-west Europe mid-April to mid-May. However, large numbers are still recorded passing through Gibraltar in May and into June (Finlayson 1992). Similarly, in east Europe and Asia the main arrivals are at the end of March–early April in the south to late April–mid-May in the north. In Japan, Barn Swallows arrive from February–March in the south to May in the north. Migration times thus depend on latitude but also on altitude; Barn Swallows arrive later and depart earlier at higher latitudes, so have a shorter breeding season, and they also arrive later at higher altitudes (Sparks & Braslavská 2001). The main movement of Barn Swallows to northern areas, however, is preceded by the arrival of a few, generally solitary birds. Exceptionally some are seen in February and early March, as in 2004 along the south and south-west coast of England and southern Scotland. Usually, the earlier individuals reach southern Europe by the end of February and north-west Europe by the end of March (Cramp 1988).

14639.qxd

24/1/06

178

3:54 pm

Page 178

The Barn Swallow

In the New World, the main spring migration through Central America is in March to May and in the West Indies and Bermuda in April to May (Brown & Brown 1999a). Although, as mentioned above, some Barn Swallows are recorded in North America in January–February, the main influx starts from late January in California to early April in the north-east and mid-May in Alaska. Peak migration periods are less variable: mid-April to mid-May in southern California and mid to late May in the north-east. The factors determining when Barn Swallows migrate are unknown, but changes in daylength, and in the weather and food supply, on the wintering grounds and on the migration route are likely to be important (Berthold 2001). High rainfall in winter is associated with good feeding conditions and improved survival for Barn Swallows (Chapter 9) and might therefore be linked to speedy completion of the moult, allowing the birds to migrate early. Møller (1994a,f ) did not find a relation between average arrival date on the breeding grounds and rainfall in the winter quarters in southern Africa, but arrival dates were more variable in years when the rainfall in March in South Africa was high. A better predictor of the timing of migration appears to be an index of green vegetation density known as the ‘normalised difference vegetation index’ or NDVI, which is based on information obtained from satellites and varies between years. A high value of the index reflects good rainfall and plant growth, and hence a probable abundance of the Barn Swallow’s food; a low value reflects poor plant growth, as a result of drought for example, and probably few insects. In a study on Italian Barn Swallows caught in consecutive breeding seasons, Saino et al. (2004a) found that Barn Swallows, of two or more years of age, arrived back earlier when the NDVI in the wintering area in western and central Africa was high, and hence feeding conditions were good (Figure 10.1). The arrival dates of younger Barn Swallows did not depend on the NDVI, however. The researchers suggested that poor feeding conditions over winter may slow the moult and hence delay departure in spring. Why there is no effect for young birds is not clear; other factors during migration or on the breeding grounds before they settle at a nest site may be more important than conditions over winter for relatively inexperienced youngsters (Saino et al. 2004a). Feeding conditions en route back to the breeding grounds are also important for survival (Chapter 9) and affect the progress of migration (Møller 2004b; Szép & Møller 2005). It is likely that the weather on the wintering grounds or early on the migration route influences the timing of migration more than that in spring on the breeding grounds, which may be markedly different, because the former will determine when and how quickly Barn Swallows migrate north. Thus Gordo et al. (2005) found that precipitation in the Sahel was a better predictor of arrival dates of Barn Swallows in north-east Spain than local weather was. In this southern area, Barn Swallows have been arriving later in recent decades, at the same time as the Sahel has been getting hotter and drier. Nevertheless, local temperatures clearly influence the timing of migration within Europe. Thus, Barn Swallows arrive earlier in Britain when March temperatures in Iberia and April temperatures in both central England and western France are

14639.qxd

24/1/06

3:54 pm

Migration and dispersal

Page 179

179

Figure 10.1. Adult Barn Swallows arrive at their Italian breeding grounds earlier when feeding conditions (measured as the normalised difference vegetation index, NDVI) in their wintering quarters were good. Vertical lines represent standard errors. Numbers are numbers of transitions between years. Closed symbols: adults; open symbols: young birds. From Saino et al. 2004a.

high, and arrival dates since 1959 show a correlation with average temperatures in central England in February to April (Sparks et al. 2001; Sparks & Loxton 2003; Figure 10.2). Arrivals elsewhere in Europe are also related to spring temperatures (e.g. Vansteenwegen 1992; Møller 1994f, 2004b; Sparks & Braslavská 2001). The progression of spring migration in Europe is probably slower than in Africa because of this dependence on local temperatures; if they meet unfavourable conditions, the birds may delay their migration northwards. Because the progression northwards depends on the prevailing temperatures, the timing varies between years. In some years in Britain, for example, much larger areas of west Wales and south-western England are reached by early April than in others. However, Barn Swallows usually reach Scotland by May in all years and so travel faster in Britain in years when they arrive late (Huin & Sparks 1998). Sparks & Braslavská (2001) also noted a faster northwards movement of late Barn Swallows in the Slovak Republic. The route taken by British Swallows follows the areas of warmest weather along the coasts of Spain and France in February and March, and then into south-west Britain, whereas in April the warm weather extends inland, allowing the birds to migrate on a broader front. The earliest arrivals in Britain, in February, also mainly come to those areas that enjoy spring temperatures early. Elsewhere, too, Barn Swallows are usually recorded after a number of days with warm weather (e.g. Samuel 1971b). In Estonia, the main arrival coincides with mean temperatures of at least 8 °C (Veromann 1981). Although the arrival of Barn Swallows in Europe is traditionally often associated with Easter or with certain Saints’ Days, arrival dates can vary by several weeks

14639.qxd

24/1/06

180

3:54 pm

Page 180

The Barn Swallow

Figure 10.2. Arrival dates (upper line) of Barn Swallows in Britain since 1959 (first sightings at coastal observatories) and the average February–April temperature in central England (˚C, lower line). Smoothed lines are also shown. Graph courtesy of Tim Sparks, CEH Monks Wood.

between years. In a German study, for example, arrival dates between 1927 and 1988 varied between 25 March and 27 April, with an average of 10 April (Radermacher 1989), and in Britain dates of arrival in Leicestershire between 1942 and 1991 varied from 15 March to 11 April (Mason 1995); Barn Swallows arrived earlier in the 1940s when springs were warm and later in the 1970s when they were cold. Mason (1995) did not find a significant relation between arrival date and April temperatures, but Sparks & Carey (1995) did find an effect of April temperatures on first arrival dates for a set of records spanning two centuries, 1736 to 1947, from Stratton Strawless in Norfolk. Between 1959 and 2003, arrival in the UK as a whole has been later in cold springs such as in 1986 and earlier in warm ones (Sparks & Loxton 2003; Figure 10.2). In Denmark, Møller (1994a, 2004b) also noted a range of arrival dates for males, with earlier arrival, relative to females, in springs with high average April temperatures. Using first arrival dates to look at changes in timing of migration with temperature can be problematic, as first dates may not be indicative of the main influx of migrants, reflecting exceptional individual birds, especially males, or meteorological events such as south-westerly gales bringing migrants with them, rather than longer-term trends in the weather. In addition, arrival dates may reflect conditions in areas outside the breeding grounds (Gordo et al. 2005). In the Stratton Strawless records, for example, Barn Swallows arrived early in 1745, even though the preceding winter had been exceptionally cold (Sparks & Carey 1995). However, changes in first arrival dates appear to reflect changes in temperature and so may be useful in understanding at least part of the population’s response to changes in climate (Sparks et al. 2001).

14639.qxd

24/1/06

3:54 pm

Migration and dispersal

Page 181

181

A major source of variation in climate is due to the North Atlantic Oscillation (NAO) which is a movement of the atmosphere between the arctic and subtropics. At one phase of the oscillation (a high NAO index) there are strong westerly and south-westerly winds across the Atlantic, giving Europe a mild, wet winter and early spring; at the other phase, there are weak west–east winds, allowing cold air from the north to penetrate Europe over winter. The NAO also has effects in North America and Africa. The NAO index has shown a marked upward trend over recent years, and may in part be influenced by increases in greenhouse gases and warmer sea surface temperatures (Hurrell et al. 2001). The influence of the NAO on migration times of Barn Swallows is not yet clear, however. A study in Norway found that migrants, including Barn Swallows, arrived earlier after a winter with a high NAO index (Forchhammer et al. 2002). However, another study (Hubalek 2003) found a relation between arrival dates and the NAO only for short-distance migrants and not for Barn Swallows in the Czech Republic. There was also no effect of the NAO on the relative arrival dates of Danish Barn Swallows of different ages (Møller & Szép 2005a). If the NAO does affect Barn Swallows’ migration time, it may do so via factors on the wintering grounds or during migration in Africa, rather than via warmer springs in Europe, as it influences vegetation productivity, and thus feeding conditions for Barn Swallows, in both the Sahelian zone (high values being linked to low productivity) and southern Africa (high values linked with high productivity; Oba et al. 2001; Forchhammer et al. 2002). Whether the winds associated with the NAO also affect Barn Swallows on migration is not known; south-westerlies and westerlies provide a tailwind which may speed migration (Sparks et al. 2001), but would not be helpful for Barn Swallows feeding while migrating. Mason (1995) did not see a long-term trend in arrival dates between 1942 and 1991 and Sparks & Carey (1995) found only a slight trend for later arrival over two centuries. However, arrival dates of Barn Swallows do seem to be affected by current increasing temperatures and are accepted by the British Government as an indicator of changing climate (Cannell et al. 1999). There is a trend for temperatures in March or April in at least parts of Europe to be getting warmer and some migrants, including Barn Swallows, are arriving earlier (e.g. Russia, Sokolov et al. 1998; Poland, Tryjanowski et al. 2002; Denmark, Møller 2004b; Britain and Scandinavia, Sparks et al. 1999; Sparks & Loxton 2003). Of 15 studies, 12 showed a trend to earlier arrival for Barn Swallows, five of which were statistically significant (Lehikoinen et al. 2004). Sparks & Loxton (2003) estimated that a rise in spring temperature of 1°C would advance arrival by two to three days. In New York State and Massachusetts, USA, too, Barn Swallows arrived significantly earlier in the second than in the first half of the twentieth century (Butler 2003). In contrast, between 1961 and 2000, Barn Swallows showed a trend towards arriving later and departing earlier in the Slovak Republic, where April temperatures have, until recently, been declining (Sparks et al. 1999; Sparks & Braslavská 2001). Barn Swallows arrive back at their breeding grounds over several weeks. In Scotland, for example, the first Barn Swallows are seen from mid to late April, but the main influx is the first two weeks of May, and some birds do not arrive until June.

14639.qxd

24/1/06

182

3:54 pm

Page 182

The Barn Swallow

Males tend to migrate and arrive on the breeding grounds before females, but their arrival dates are also more variable (Møller 1994a). In the Mediterranean, for example, one study noted a median trapping date for male Barn Swallows of 27 April and for females 30 April (Spina et al. 1994). In Denmark, males have arrived on average on 16 May (range 23 April to 2 July) and females on 20 May (range 26 April to 1 July), with males arriving on average 4.8 days before their mates (Møller 1994a). However, Møller (2004b) found that, since the early 1970s, males, but not females, have been arriving earlier, so the difference in arrival date between males and females has increased. The birds that arrive early are those that are in good condition: males with a good immune response arrive early, whereas those with lots of parasites arrive late (Møller et al. 2004b; Chapter 4) and long-tailed males arrive earlier than short-tailed ones (Møller 1994f ). There is also a difference between age classes, one-year-olds and those five or more years old returning later than two- to four-year-olds (e.g. Loske 1994; Møller & de Lope 1999). Older males in Denmark arrive about six days earlier than first-year males, and older females about four days earlier than first-year females (Møller & Szép 2005a). In Scotland, two-thirds of birds arriving on or before 1 May were at least two years old, whereas those first caught after May were usually first-years (Thompson 1992). The effect of feeding conditions on survival in turn impacts on the spread of arrival dates within a population; poor-quality individuals may survive in particularly good feeding conditions but arrive late (Szép & Møller 2005). Similarly, high early spring temperatures on the breeding grounds increase the difference in arrival dates between old and young birds (Møller & Szép 2005a). There are both costs and benefits to arriving back early on the breeding grounds. The clear disadvantage is that the weather may still be, or suddenly turn, bad, with late cold snaps, and even snow. Severe spring weather can cause high mortality in hirundines (Chapter 9). On the other hand, there are advantages (Møller 1994f; Chapter 4). The mating success of males depends on their arrival date; early males are more likely to get not only a mate but also a high-quality mate and to sire more chicks than late males do. Because of these benefits, there is competition among males to return early in order to get a good territory and be ready to mate when the females arrive, especially when mortality is high on migration and mainly those in the best condition survive. Females, in contrast, which choose a mate from those males available on arrival, are under less pressure to return so early. Thus Møller (2004b) found that males, but not females, arrived earlier on the breeding grounds when feeding conditions in the North African part of the migration route were poor and survival of males was low. The survivors are generally long-tailed males in good condition, which are also better able to cope with adverse weather in spring on the breeding grounds than are short-tailed males in poorer condition (Møller 1994a,f; Møller & Szép 2005b). Amelioration of spring temperatures because of current climate change makes early arrival even less costly and so also allows males to return earlier (Møller 2001a, 2004b). However, there is likely to be a limit to how early Barn Swallows can return to the breeding grounds, despite better conditions in

14639.qxd

24/1/06

3:54 pm

Page 183

Migration and dispersal

183

the spring, because of the requirement to finish or almost finish the moult before departure (Møller 2001a).

MIGRATION ROUTES Surprisingly, considering that Barn Swallows are so well known as migratory birds, there has been only one attempt to investigate how they find their way to and from the winter quarters. Giunchi & Baldaccini (2004) tested juvenile Barn Swallows, trapped at a roost site in Italy during autumn migration, in Emlen funnels (specially designed cages in which the preferred direction of movement of birds can be measured), both in the ambient and in a ‘shifted’ magnetic field, in which magnetic north was changed to correspond to the geographical west. Under clear skies, the Barn Swallows ignored the manipulation of the magnetic field and tended to head for the brightest part of the funnel. In overcast conditions, however, they changed their preferred direction (northwards) and headed towards geographical west, in line with the shifted magnetic field. This shows that they can use a magnetic compass, which is a widely used mechanism for orientation among birds. This sort of compass is based on the inclination of the magnetic field lines, which allow the birds to distinguish between ‘poleward’ and ‘equatorward’ (Berthold 2001). As Giunchi and Baldaccini point out, why the juveniles oriented northwards under overcast skies at this time of year is not clear; one possible explanation is that they might have been orienting towards the roost sites where they were caught. Although Barn Swallows are able to use magnetic information, it is likely that they use other cues as well, perhaps the position of the sun, or the pattern of polarised light in the sky on overcast days; they probably also use landmarks or even olfactory cues when near familiar areas such as the breeding or wintering sites. In addition, Barn Swallows may follow topographical features, which may help them maintain the correct course. The routes Barn Swallows take are much better known than how they know where to go. Ormerod (1991), for example, analysed the movements of Barn Swallows in autumn in Britain and Ireland. Birds hatched that year at first moved in any direction, averaging 25–32 km over ten days when moving in northerly or westward directions, but during September and October, the peak of migration, their movements became concentrated to the south-east; some adults also moved north or westwards in August and September. Juveniles from southern Europe, where breeding is earlier, that have moved northwards after fledging, aided by south-westerly winds, may account for the juveniles occasionally recorded in Britain in April and May, before British Barn Swallows have bred (e.g. Glue 1994). Barn Swallows from eastern Britain travel down the eastern side of the country and western birds the western side (e.g. Lynch 1982). When Ormerod (1991) analysed movements made within ten days of ringing, the data showed that the birds moved further each day within Britain as the autumn progressed, from an average of

14639.qxd

24/1/06

184

3:54 pm

Page 184

The Barn Swallow

2.9 km per day in July to 26.3 km in October, individuals moving south and east also moving most rapidly. However, individuals recaptured within a day did not move faster with time, suggesting that Barn Swallows stop less frequently in October. They may also be more likely to head in one direction then rather than wander. Distances moved over a single day (71 km) were two or three times that measured per day over ten days, suggesting that birds travelled in stages, stopping at a site for several days before continuing the migration. As the season progresses they may stay less time at any one site, thus appearing to travel faster. Individuals from westernmost Europe, including Sweden and Norway, head for the Iberian Peninsula and the Mediterranean, from Britain taking about 4–16 days (Mead & Clark 1987; van den Brink & van der Have 1993; Mead 2002). From Britain and Ireland, they cross the Channel to the French Biscay coast then by way of the northern edge of the Pyrenees to the Mediterranean coast. Many avoid a long sea crossing by crossing into North Africa from southern Spain and across the Strait of Gibraltar. They then cross the 1,500 km of the Sahara and Sahel region on a fairly broad front, mainly overland and to the west of the Greenwich meridian, and continue down to the wintering areas mainly by way of Nigeria and the Congo Basin. There is little evidence that they avoid the desert by flying along the coast (e.g. Moreau 1961). From further east in Europe, for example Denmark, Barn Swallows travel south over the Alps or south-west to the Iberian Peninsula (Møller 1994a), while others, such as those from Italy, travel straight across the Mediterranean. Eastern populations travel down through the eastern Mediterranean and the Middle East. The return migration in spring is more direct (Mead 2002). In West Africa, for example, there are then more records from Algeria and Tunisia than in the autumn and more from the central Mediterranean between the Balearics and Italy. British Barn Swallows move north through Europe along the eastern coast of Spain and the western coast of France, entering Britain from the south-west and moving northeast (Huin & Sparks 1998). However, in years when Barn Swallows arrive late, the migratory axis in Britain is more south to north (Huin & Sparks 1998). In central Asia, Barn Swallows probably mainly travel down through Pakistan into East Africa or south into the Indian sub-continent. Their return route in spring is not known, but from Africa, because of the prevailing winds, they may fly on a more northerly route via Iraq and Iran; spring migrants may also concentrate in the lowlands and avoid mountains where temperatures may still be unfavourable (Gavrilov et al. 2002). Barn Swallows from eastern Asia may migrate inland or along the coast. Some Japanese, Korean and east Siberian Barn Swallows follow the Pacific island arc south through Taiwan to the Philippines, Malaysia or Indonesia; others travel inland, although there is some mixing of birds between the two flyways (McClure 1974). From North America, Barn Swallows mainly travel down through Central America, keeping to the coastal lowlands rather than mountains inland, but some have been recorded crossing the Gulf of Mexico and Caribbean and migrants are often seen in the West Indies and Bermuda (Brown & Brown 1999a). Migrants occur on a broad front in northern South America, from Colombia to French

14639.qxd

24/1/06

3:54 pm

Page 185

Migration and dispersal

185

Guiana. Whether the spring migration is more direct, as in Europe, is not known, but fewer Barn Swallows are seen in Bermuda in spring than autumn.

BEHAVIOUR ON MIGRATION Barn Swallows migrate in small (a few tens of birds), loose flocks or chains of birds. Sometimes these small groups come together, however, to form large streams of hundreds or even thousands of birds both while in flight and at stopping places such as oases in deserts (e.g. Lyuleeva 1973). Barn Swallows will join migrating flocks of other species, especially other hirundines, but also other birds such as swifts and bee-eaters. The loose flocks of Barn Swallows give each individual space to hunt for insects en route. This way of feeding also means that Barn Swallows usually migrate by day rather than by night and generally fly at low altitudes, less than 100 m and often just a few metres above the ground. In the autumn, adults seem to travel more quickly than juveniles, which migrate earlier and later in the day than adults (Gatter & Behrndt 1985). Barn Swallows travel over a variety of habitats from wetlands to farmland and towns, but especially over lowland and coastal areas. While on migration they often follow topographical features such as coastlines and rivers (e.g. Slud 1964). They probably avoid less profitable feeding areas such as dense forests and high mountains as much as possible, but they do cross mountainous areas and have been recorded up to 6,400 m in Nepal (Grimmett et al. 1998). Good roosting sites, such as large reedbeds, along the route are likely to be important as stopovers where Barn Swallows can fatten up before continuing migration, especially when the birds need to cross deserts or water, where they cannot feed en route (Pilastro & Spina 1999). The weather affects Barn Swallow migration in several ways (e.g. von VietinghoffRiesch 1955; Lyuleeva 1973). Barn Swallows prefer to migrate in a head wind or cross wind. In such a wind they can fly a metre or so above the ground, where wind speed is lowest, and hunt insects. In a tailwind, hunting is difficult because of wind turbulence close to the ground; even though the Barn Swallow’s flight is adapted to turbulent conditions (Chapter 2), a sudden drop in wind speed could make the bird stall. Chasing insects into the wind is easier. If the wind is blowing in the same direction as the Barn Swallows are migrating, they may stop migrating temporarily, or fly with it at higher altitudes for a while, probably without feeding, or they may turn and fly against it. These reverse migratory movements are most common in the evening, probably when the birds are looking for feeding and roosting sites. They are also more common in the autumn when the migration is more leisurely than in the spring. The wind has an additional effect on the distribution of insects, and Barn Swallows may have to seek out shelterbelts in windy conditions to find them. Wind can also be a problem when Barn Swallows cross stretches of water, as it can blow them off course; one British Barn Swallow was recovered 320 km

14639.qxd

24/1/06

186

3:54 pm

Page 186

The Barn Swallow

south-south-west of Ireland in strong south-easterly winds. If they are blown out to sea they can be engulfed by high waves or just weaken and die before reaching land again. Barn Swallows at sea will perch on ships, but are usually too enfeebled by then to survive (Yunick 1977). Even over relatively short stretches of water, winds can vary in direction and intensity, making flight more difficult and costly. On the other hand, tailwinds may be helpful for small birds crossing large inhospitable areas such as the Sahara (Biebach 1992). Although helpful to Barn Swallows when feeding, head winds, which are common in the Sahara in spring, may make the desert crossing more difficult (Moreau 1961). Movements of migrating Barn Swallows are more intense when temperatures are high (e.g. Lyuleeva 1973). Low temperatures make insects scarce and more localised at low altitudes, forcing Barn Swallows to feed lower themselves and to change the direction of flight to seek out warmer sites, such as dunes rather than forest. Rain and mist have similar effects, sometimes bringing the birds to a temporary halt. Migrating Barn Swallows often gather in large numbers over waterbodies to feed in inclement weather and, in spring, are often recorded in such habitats before they begin breeding. Severe weather can delay and disrupt migration. In late September and October 1974, for example, instead of the usual high pressure zone in Europe, depressions moved south-south-west over the North Sea, followed by cold northerly winds. Many hirundines starting out on their journey were caught out and migration in the Alps almost ceased; thousands of hirundines moved into south-east England from the continent ahead of the depressions and tens of thousands died (Bruderer 1979). Adverse weather early in the year in the winter quarters can also delay the return migration in spring, while the weather in Europe, as described above, determines when the Barn Swallows arrive in the breeding areas. Cold weather can interrupt settlement of the breeding areas: in May 1998 in the Azov region of southern Russia, recently arrived Barn Swallows disappeared from the farmland and villages and retreated to forested areas, particularly hawthorn thickets, where they stayed for several days until the weather improved (Zabashta 2000). Barn Swallows fly at a range of speeds while migrating, as they tend to forage at the same time (Chapter 2). Distances travelled in a day vary markedly, especially at the start of migration. In Britain, Ormerod (1991) found that Barn Swallows would travel up to 194 km per day, but sometimes less than 30 km per day. For longer stretches of the migration route, Barn Swallows have been recorded making trips of more than 5,600 and 4,800 km in two months, 80–93 km per day (Kang 1971); van den Brink et al. (1998) recorded a Barn Swallow flying from Paris to Ghana in 27 days (188 km per day) and Pilastro & Spina (1999) reported one that travelled an impressive 3,028 km in seven days (433 km per day) between Italy and Niger. Estimates for the return journey north in spring range from five weeks to three months, about 100–300 km per day (e.g. Mead 1970; Huin & Sparks 1998), and Rowan (1968) noted two from South Africa flying about 8,500 and 12,000 km in 34 days, about 250 and 350 km per day, respectively. Barn Swallows can travel considerable distances in a day; breeding birds displaced from their nest site have been recorded flying about 400 km per day (Rüppell 1934).

14639.qxd

24/1/06

3:54 pm

Page 187

Migration and dispersal

187

FAT RESERVES FOR MIGRATION Since Barn Swallows feed while migrating, they do not need to build up large fat reserves beforehand. Nevertheless, as the weather, and hence their food supply, is unpredictable, and in any case is likely to deteriorate in the autumn, they put on some fat reserves to tide them over adverse periods. In addition, they put on large amounts of fat before flying over areas where insects are unavailable, such as large expanses of water or desert. Fat is deposited under the skin, around the internal organs and within the muscles and liver (Lyuleeva 1973). The pectoral muscles are also much larger at this time than during the breeding season. Barn Swallows increase their weight after breeding. For example, the mean weight of Barn Swallows at a roost in Wales increased by 0.03 g/day on average between July and September (body weight range 18.1–22.3 g; Ormerod 1989), with some evidence of an accelerated increase in September. By the second week of September they had gained 2–3 g, or 10–15% of mean August weights. The mean weight at the roost varied greatly from day to day, as wind speed, duration of rainfall and maximum daily temperature also affected the weight of birds (explaining nearly half the variation in body mass), presumably by affecting the availability of insect food. Similar increases in weight after breeding are seen elsewhere; for example, the Tay Ringing Group in Scotland recorded an increase in weight of adult Barn Swallows from an average of 20.1 g in the first half of August to 23.7 g by the end of September, again with a noticeable increase in September (Lynch 1982). Preliminary results from the BTO’s Swallow Roost Project show that in Britain and Ireland as a whole, Barn Swallows put on an average of 1–2 g between late July and late September (BTO News September–October 2005, pp. 6–7). The seasonal increase may partly reflect a need for adults to gain weight after reaching low weights after breeding, particularly as an insurance against worsening weather and scarcer food at these high latitudes, and an increase in the foraging efficiency of juveniles, but the birds may also be putting on some fat reserves during this early stage of migration, as the birds gain weight at the time they start to head south-east and to travel more rapidly (Ormerod 1989, 1991). Barn Swallows leave northern Europe at a relatively low weight, however, arriving in southern Europe from August onwards, where they finish any body and wing moult they may have started, and probably only then fatten up for the long trip across the Sahara desert. Preliminary results of the EURING Swallow Project from 18 countries in Europe showed that, generally, Barn Swallows start to increase in weight considerably from the beginning of September with higher average values in southern areas (Pilastro & Spina 1999). Relatively few Barn Swallows caught in northern Europe in September–October weigh more than 24 g (e.g. 0.9% in Finland) compared with those in southern Europe (8.9% in Italy). Less clement weather in northern Europe may prevent Barn Swallows putting on fat at a high rate; alternatively there may be less need for large reserves while the birds are travelling at these latitudes.

14639.qxd

24/1/06

188

3:54 pm

Page 188

The Barn Swallow

In contrast, Barn Swallows at a roost in northern Italy did not start to gain weight until late August; juveniles even declined in weight (Pilastro & Magnani 1997). When they did start to gain weight they also did so at a high rate: 0.2 g/day for adults and 0.14 g/day for juveniles, reaching 24 g or more. In Italy, Barn Swallows thus have a longer post-breeding period before preparing for migration. Why this is so is unclear. It may be related to the warmer, drier climate in southern Europe which may both make it less necessary for Barn Swallows to put on fat as insurance against inclement weather immediately after breeding and make it possible to accumulate fat at a high rate ready for migration. It may also give Barn Swallows more time for moulting before migrating, as doing so during migration would be costly and would reduce the distance they could fly using energy stores alone. In southern Europe, juveniles put on more fat than adults in the post-breeding period (July/August), but less in September just before migration (Pérez-Tris et al. 2001; Rubolini et al. 2002b). In addition, during the period immediately after breeding, Barn Swallows in an Italian study weighed more in cool or windy weather, whereas just before they migrated they weighed more in warm, humid conditions; this suggests that the costs and benefits of carrying fat reserves change during this period (Pilastro & Magnani 1997). After breeding, fat stores may be needed to tide birds over when the weather is poor, especially by juveniles which weigh more than adults at this stage, whereas in good weather a low weight is preferable, perhaps to improve the bird’s ability to escape from predators (McNamara & Houston 1990). Adults also moult their body feathers after breeding and may be limited in how much fat they can put on at the same time. In contrast, before leaving for North Africa, putting on fat for fuel reserves is paramount and the birds take the opportunity to put on weight when the foraging conditions are good; at this stage adults have more fat than juveniles, perhaps because they are more efficient at foraging (Pilastro et al. 1998; Pérez-Tris et al. 2001; Rubolini et al. 2002b). In Italy, Rubolini & Schiavi (2002) also found that long-tailed males have larger fat stores than short-tailed males, both after breeding and before migration. They may be able to put on fat more efficiently and thus have more available to use on migration at times when foraging is difficult. In addition, the increase in fat score in relation to increasing tail length was similar in males and females in this study, suggesting that individuals of either sex with long tails can put on fat at a high rate. Before crossing from Europe into Africa, Barn Swallows can put on as much fat as other trans-Saharan passerine migrants, some 30–40% of lean body weight. Pilastro et al. (1998) calculated the mean fat reserves of Barn Swallows at 24 roosts in Italy in early September to be 1.85 g for juveniles and 2.87 g for adults, and of the 25% heaviest birds, 4.2 g and 5.4 g (24% and 31% of lean body weight, 60% for the heaviest), respectively. Pilastro & Magnani (1997) calculated similar values for a roost in northern Italy later in the season, with the heaviest birds having fat reserves of about 40% of lean body weight. Adults have more fat than juveniles, 41% versus 31% of lean body weight, respectively (Rubolini et al. 2002b). In contrast, Barn Swallows that had migrated across the Sahara and Mediterranean in spring, probably flying non-stop for 14–16 hours, had only 0.5 g of fat and weighed only

14639.qxd

24/1/06

3:54 pm

Page 189

Migration and dispersal

189

13.4 g on average (Schwilch et al. 2002). Bairlein (1985) similarly recorded mean weights of 17.5 g and 15 g for Barn Swallows before and after the Saharan crossing. When they are close to exhausting their fat reserves, Barn Swallows, and other migrants, break down protein from their breast muscles and gut (Schwilch et al. 2002). This appears to happen, for example, when birds are moulting at the same time (Pérez-Tris et al. 2001) Pilastro & Spina (1999) calculated that Barn Swallows with a weight of 24 g or more should be able to cross the Mediterranean and Sahara on a single endurance flight without refuelling. The evidence also suggests they make the trip in one go: Barn Swallows are not often seen at stopovers in the desert and weights of Barn Swallows recorded in Algeria were similar to those in southern Europe, suggesting that no further refuelling takes place (Bairlein 1988; Biebach et al. 1991). How much fuel they take on seems to depend on whether they are crossing both the Mediterranean and Sahara from Italy or taking the shorter trip from Spain, and avoiding the sea. Very fat birds, weighing more than 24 g, were caught particularly in Italy, whereas those travelling down the Iberian peninsula were lighter. Italian birds put on more fat (37% of lean body weight) than those in Spain (25% of lean body weight; Rubolini et al. 2002b; Figure 10.3). This is equivalent to an extra 1.5–2.0 g of fuel which could last for a distance of about 800 km. The Italian Swallows in the above study have to travel about this distance over the Mediterranean Sea, about twice that covered by the Spanish birds. The extra fuel may be needed for flying in unpredictable winds when crossing the sea (Moreau 1961). Whether Barn Swallows on more westerly routes take shorter flights with more frequent stopovers than those in Italy is not clear, however, and further data on geographical comparisons are needed (Pilastro & Spina 1999). Once the Barn Swallows are in their winter quarters, their body weights vary, probably depending on feeding conditions, especially rainfall (Møller et al. 1995b). In Botswana, for example, Barn Swallows weighed an average of 20 g when rainfall was high and 17–19 g during droughts, with some birds weighing as little as 14 g (van den Brink et al. 1997, 2000, 2003); and, at a roost in Namibia, Anders Møller (pers. comm.) recorded average weights of 17 g before and 22 g after the rains started. Barn Swallows also increase their weight, by 2–4 g, before migrating north (van den Brink et al. 1997, 2000). Whether the relatively low weights during the winter are strategic to reduce predation risks is unknown (van den Brink et al. 2003).

MOULTING Barn Swallows moult once a year after breeding, sometimes starting before migrating, but the main part of the moult takes place in the winter quarters, starting in mid-September to mid-November and ending in late January to late March. Because Barn Swallows have to fly efficiently to catch their food, the moult has to be a slow process, taking 4.5 to 6.5 months (Cramp 1988; Jenni & Winkler 1994). For Barn Swallows breeding in northern areas, there is not time to moult after breeding and

14639.qxd

24/1/06

190

3:54 pm

Page 190

The Barn Swallow

Figure 10.3. Barn Swallows that must cross both the Mediterranean and Sahara from Italy put on more weight before migrating than those that cross only the Sahara from Spain; (a) adults and (b) juveniles. Closed symbols: Italy; open symbols: Spain. PB: post-breeding phase; PM: pre-migratory phase. From Rubolini et al. 2002b.

before the deteriorating weather forces them south, nor can they start when they need full efficiency for feeding chicks or fledglings. Those breeding in southern areas, however, are able to start before migrating. The moult progresses in stages: first the body feathers and wings; then, when the fifth primary is in moult, the tail feathers start. These are only slowly replaced and the outer primaries and tail feathers may still be growing when the bird returns to its breeding area (Jenni & Winkler 1994; Møller 1994a). Despite arriving at the breeding site later than long-tailed males, males with short outermost tail feathers are more likely still to be growing theirs on arrival (Møller 1994a), perhaps because short-tailed males take longer to moult in the winter quarters (Møller et al. 1995b). The body moult starts with the back and rump, progresses to the breast and neck and ends with the head feathers. The blue-black feathers of the upperparts and breast-band are glossy when fresh but become duller and may develop white specks when worn or moulting. The primaries are moulted from the inner to the outer ones, the secondaries from the outer ones towards the body. The first secondary and fifth

14639.qxd

24/1/06

3:54 pm

Migration and dispersal

Page 191

191

primary are replaced at about the same time, as are the last secondary and last primary. The wing coverts moult with the main wing feathers. In a study in Botswana, the first four primaries were renewed by late December–early January and the last two were in moult by the end of January; the wing moult was estimated to last 120–130 days in a normal year and 155–190 days in a drought year (van den Brink et al. 1997, 2000, 2003). The tail moult starts from the centre but, in adults, the outer feathers may be moulted before the penultimate or even antepenultimate ones; individuals that return to the breeding areas with tail feathers still growing will thus still have fully grown streamers which they need for foraging and for sexual display (Møller et al. 1995b; Chapter 2). In Botswana, the tail moult started in late December and was estimated to last 80–105 days, finishing in mid-February to mid-March (van den Brink et al. 1997, 2000). In contrast, at roosts in Ghana, birds arrived already in active wing and tail moult about a month advanced over those in Botswana and probably departed earlier: the birds wintering here include southern European ones, which return to the breeding grounds in February, earlier than the northern birds that winter in Botswana (van den Brink et al. 1998). The feathers in the wings and in the tail are moulted symmetrically in most birds, so that their flying ability is not unduly impaired; however, over 30% caught in South Africa moulted asymmetrically (A.P. Møller, pers. comm.). Although the main moult takes place in the winter quarters, some birds do start moulting while still on or near the breeding grounds particularly, in the case of adults, moulting body feathers and sometimes inner primaries, wing coverts or even an inner tail feather. This partial moult can continue into migration. The moult is then suspended while the birds cross North Africa where foraging is too difficult to sustain both migration and moulting. There are also a few records of birds, in Britain and Iraq, starting primary moult while apparently breeding (Richards & Goodwin 1950; George 1976). Only a small percentage of birds moult one or more primaries early (3% recorded in Switzerland and Belgium, 7% in Tien Shan, 10% in Sweden and Germany, 19% in Spain: Cramp 1988; Jenni & Winkler 1994; 9% in Italy, Pilastro et al. 1998). Usually only one or two primaries are moulted at this time, but four has been recorded and one bird caught in Switzerland had also started moulting its secondaries (Jenni & Winkler 1994). It is more common for Barn Swallows to start the body moult early. In Italian and Spanish studies, the proportion of Barn Swallows that were in moult increased immediately after the breeding period, peaking at over 80% in August, and then declining during the pre-migratory period to about 20% by the end of September (Pérez-Tris et al. 2001; Rubolini et al. 2002a); the proportion in moult also increases from north to south and from west to east (Rubolini 2000, cited in Rubolini et al. 2002a). In addition, there is a sex difference. In the Italian study, more females than males were in moult and the moult period lasted longer, with few males but about 20% of females still in moult in September (Rubolini et al. 2002a). Females may start later and need new feathers more than males do, because the females’ feathers are likely to suffer more abrasion during incubation and chick-brooding in the nest (Rubolini et al. 2002a).

14639.qxd

24/1/06

192

3:54 pm

Page 192

The Barn Swallow

Most juveniles wait until they are in their winter quarters before moulting, but some start the body moult, particularly of the orange feathers on the head, while in the breeding areas. A few also start primary moult, but this is less common than with adults. In Italy, 21% showed some body moult, 3% intense body moult and 0.4% primary moult, with relatively more active than suspended moult than among adults (Pilastro et al. 1998). North of the Mediterranean, however, few juveniles have been recorded with new or growing flight feathers (e.g. Jenni & Winkler 1994; van den Brink 1994). Wing coverts are also rarely moulted early. When juveniles do moult before migration, they seem to do so earlier in the season than adults; the proportion that are in moult declines from about a third in July–early August to about 15% in September (Pérez-Tris et al. 2001; Rubolini et al. 2002a). In the winter quarters, juveniles moult rather later than adults, up to six weeks in central Africa and Asia and two to three weeks later in southern Africa (Cramp 1988; Jenni & Winkler 1994; Brooke 1995; van den Brink et al. 1997, 2000). The main moult in other migratory populations also occurs in the winter quarters, with possibly some early starters. Adults in southern populations in North Africa, perhaps in Iraq and Iran, and parts of China start to moult after breeding in June or July and finish in the winter quarters. Local and altitudinal migrant and resident populations moult even earlier, starting in late April–June and finishing in September–November (Stresemann & Stresemann 1968; Pimm 1972; Cramp 1988). Juveniles in resident populations moult soon after fledging (Cramp 1988). In North America, the moult also occurs mainly in the winter quarters, adults replacing their flight feathers in October–February and juveniles in November–April, but it can start earlier (Pyle 1997). The speed of the wing and tail moult differs between males and females and between adults and juveniles, and it also varies within each sex. In a study in Namibia in January, the moult of male Barn Swallows was more advanced and was progressing faster than that of females, while juveniles were the least advanced (Møller et al. 1995b). Within the sexes, the moult was more advanced and faster for males with long, symmetrical tails (the most attractive to females) and for females with short, symmetrical tails. Individuals judged to be in good condition (by an index based on weight in relation to size and weather) were also those with the most advanced moult, although the relation was weaker for females and juveniles than for adult males. Infestation with parasites, on the other hand, had little, if any, effect on the speed of moult. Juveniles lag behind adults in starting primary moult but moult these feathers more quickly, whereas tail moult is faster in adults (van den Brink et al. 1998, 2003). The speed of moult also depends on environmental conditions. In Botswana, the moult progressed fastest when rainfall and roosting habitat were abundant, at an intermediate rate when roost sites were scarcer, and slowest during a drought when few roost sites were available (van den Brink et al. 1997, 2000). Italian males also grew longer tails and wings, and females grew longer tails, when feeding conditions over winter were good (Saino et al. 2004c). Moult is thought to require a lot of energy (e.g. Murphy 1996) and may be incompatible with other energy-demanding activities such as migration. Studies have found

14639.qxd

24/1/06

3:54 pm

Page 193

Migration and dispersal

193

differences in weight and condition between moulting and non-moulting individuals at roosts, but whether this indicates a trade-off between moulting and fattening for migration is not clear. Thus, juvenile Barn Swallows after fledging and before migration, and adults during the pre-migratory period, that are in active body or primary moult have lower fat scores than non-moulting individuals (Pilastro et al. 1998; Pilastro & Spina 1999; Pérez-Tris et al. 2001; Rubolini et al. 2002a). Before migration, moulting individuals in a study in Spain were still in good condition, as measured by lean body weight, whereas by September, when migration was well underway, they were in poor condition (Pérez-Tris et al. 2001). Moulting Barn Swallows on average weigh 1–2 g less than non-moulting ones and so, with less fuel, cannot fly as far without feeding, about 500–1,000 km less (Rubolini et al. 2002a). Adults probably have a more restricted period than juveniles in which they can get enough energy to moult (Pérez-Tris et al. 2001): they may need time to recover condition after breeding and also cannot afford to overlap moult and migration. Juveniles may be able to start earlier because they do not have to recover from the rigours of breeding. Starting moult before the southward migration may be beneficial, however, for several reasons. Juveniles may benefit from improved insulation, adults may need to replace feathers that became worn or damaged during the breeding season, and an early moult means a shorter moulting period in the winter quarters, which may improve winter survival, and perhaps allow the birds to finish the moult and to return to the breeding grounds early in good condition (Jenni & Winkler 1994; Pérez-Tris et al. 2001).

DISPERSAL When they become independent, young Barn Swallows move away from their nest sites, but, as mentioned above, not necessarily in the direction of their future migration. There are several explanations for this. Juveniles might just be wandering while feeding, and moving upwind while doing so (R. Spencer, cited in Ormerod 1991; Ziel´nski & Ba´nbura 1995); they might be avoiding competition from adults; or they might be familiarising themselves with the general area and the local Barn Swallow population to aid navigation on the return migration or to locate suitable roost sites or breeding sites for the following year (Mead & Harrison 1979; Jarry 1987; Baker 1993; Pilastro & Magnani 1997). Juveniles are often seen on farms and entering buildings other than their natal site (e.g. Thompson 1992; Ambrosini et al. 2002b; Safran 2004). Although they occasionally obtain food from other pairs when they do this (Chapter 8), the main reason may be to prospect for breeding sites. First-years have been found breeding at non-natal sites that they had visited the previous year (e.g. Jarry 1987; Thompson 1992) and Møller (pers. comm.) found that local recruitment by fledglings caught at his Danish site was over twice as high as that for chicks ringed at the site. However, movements by adults in non-migratory

14639.qxd

24/1/06

3:54 pm

Page 194

194

The Barn Swallow

directions suggest at least some such movements by juveniles are linked to, for example, finding roosts rather than familiarisation with an area (Ormerod 1991). On returning to the breeding area in spring, first-year Barn Swallows settle away from where they were hatched, whereas adults usually return to the site they used the previous year, males more so than females. There have been numerous studies, on both small and large scales, following local populations of Barn Swallows between years and typically only a few per cent return to the place they were ringed as chicks (e.g. 0.4%, Anthony & Ely 1976; 0.9%, de Lope Rebollo 1983; 2%, Mason 1953; 2–3%, Vansteenwegen 1988). However, return rates do not tell us what happened to those birds that did not return: whether they died or moved elsewhere. Ringing studies suggest that young Barn Swallows usually disperse only a few kilometres from their natal site, sometimes to the same farm or to a nearby group and that males move less far than females (Table 10.1); males occasionally even return to the building where they hatched (Brombach 2004). The observed distances are biased by the size of the study area, however, and actual dispersal may be greater than indicated by these studies. Some very long natal dispersal distances are known: for example 360 km in Britain, 410 km between Germany and the former Czechoslovakia, and a Belgian bird was found breeding in Morocco (Glutz von Blotzheim & Bauer 1985). Table 10.1. Locality

Examples of dispersal distances between seasons of juvenile and adult Barn Swallows. Distance, median or mean (km)

Range (km)

No. of birds

Source

7.0 (total) 1.0 (males) 11.0 (females) 1.8 (males) 3.8 (females) Not given 0.7 (males) 2.5 (females) Not given 6.4

0–261

435

Mead 2002

50 77 55

Windig & Florus 1997 Weggler & Widmer 2000 Bauer & Heine 1992; Böhning-Gaese & Bauer 1996 Loske 1994 Brombach 2004 Jeromin 1999

et al. 1998). Local increases have also occurred, although infrequently reported, perhaps because increases are thought less newsworthy rather than because they are rare: in Oldisleben, Germany, for example, the population rose from 42 breeding pairs in 1988 to over a hundred in 2000, possibly because stabling for horses provided new nest sites (Röse 2001). In Britain, the population size is about 726,000 pairs (BirdLife International 2004). There were local reports of declines in the nineteenth and twentieth centuries (e.g. Gladstone 1910; Parslow 1973), but recent population trends have been variable, increasing in 1962–1968, 1974–1978 and 1984–1989, decreasing in 1969–1973, 1979–1983 and 1990–1994, and showing no overall significant trend between 1964 and 1998 (Gibbons et al. 1996; Siriwardena et al. 1998a, b; Robinson

14639.qxd

24/1/06

200

3:54 pm

Page 200

The Barn Swallow

Figure 11.2. Population trend of the Barn Swallow in England for 1966–2003 from the Common Birds Census/Breeding Bird Survey. The index (solid line) was set at 100 in 2000. The continuous line is the smoothed CBC/BBS trend for England and the confidence limits are 85% limits. Data for 2001 are missing because foot-and-mouth disease prevented surveys being done. Source: Baillie et al. 2005.

et al. 2003; Figure 11.2). The method used to monitor populations during much of this period, the Common Birds Census, was in some respects unsuitable for recording Barn Swallows; for example, it did not include suitable habitat such as towns and villages and was designed for more territorial species. In 1994, this method was replaced by the Breeding Bird Survey which has wider coverage and may be better for recording Barn Swallows. Since 1994, this method has shown a significant population increase of 10%. Both methods, however, revealed regional variations, with declines in the east and increases in the west; from 1994 to 2002 there has been a significant increase in Wales and south-western England and a significant decrease in eastern parts of Britain (Raven et al. 2003; Evans & Robinson 2004). On a local scale, too, there is evidence of British populations increasing, decreasing and remaining stable. On 47 Common Birds Census plots with data for at least 20 years, populations increased significantly on eight, declined significantly on 11 and there was no change on the remainder (Robinson et al. 2003). Similarly, at eight sites in England, four had increasing populations and four had declining ones (Evans et al. 2003c). In Eastern Europe and Asia, population changes are less well known. Barn Swallows have increased their range in some areas, such as the lower Amur basin (Babenko 2000), but declines are also known, such as in Kazakhstan in the 1990s (Berezovikov & Anisimov 2002). In Russia and eastern Poland, populations may also be in decline (e.g. Mal’chevskiy & Pukinskiy 1983; Konstantinov et al. 1996). In parts of the USA, especially the north-east, Barn Swallows declined in the late 1800s, possibly because of an increase in numbers of House Sparrows which destroy Barn Swallow nests (Chapter 9), but the North American population has expanded

14639.qxd

24/1/06

3:54 pm

Page 201

Populations

201

considerably in the late nineteenth and especially the twentieth centuries, both north and south, because of increased nesting opportunities (Chapter 6; Brown & Brown 1999a). Barn Swallows have increased their range in California, Arkansas and Tennessee and moved southwards into Mississippi, Alabama and Louisiana (Brown & Brown 1999a). In Tennessee, for example, the first nest was found in 1893 and Barn Swallows were present throughout the state by 1966 (Nicholson 1997). They first nested in Florida in 1946 and numbers increased rapidly in the 1970s; they have nested throughout the state to Key West, although they still occur in small numbers in the south (Florida Fish and Wildlife Conservation Commission 2003). Numbers have also increased in North and South Carolina and Georgia (Brown & Brown 1999a). Barn Swallows have also moved further into eastern and northern North America. In eastern Canada, for example, they probably nested only in southernmost areas in the nineteenth century, but when the railways were built and new towns constructed alongside them the Barn Swallows followed them north. By the 1930s they had reached Quebec and by the 1950s most of Ontario; since the mid-1970s they have started nesting along the James Bay and Hudson Bay shorelines. Between 1966 and 1994, numbers increased in the United States but decreased in Canada (Price et al. 1995). From 1966 to 2003, however, there was an overall, but slight, decrease in the United States, especially in the north-eastern and northwestern states, and a larger decrease in Canada (Sauer et al. 2004). There was still a trend of increasing numbers in south-eastern states, in particular Alabama, Arkansas and Georgia. Since at least 1980, Barn Swallows have also bred in part of their winter quarters in Buenos Aires Province in Argentina, and are expanding their range there (Petracci & Delhey 2004).

FACTORS AFFECTING POPULATIONS Environmental conditions Møller (1989a) found that, for his Danish population, most mortality (averaging 61% over 18 years) occurs outside the breeding season and this is independent of population density. Environmental conditions in the winter quarters and on the migration route can thus have a major impact and are probably the main influence on Barn Swallow populations (Baillie & Peach 1992; Chapter 9). The decline in the Danish population in the 1980s and 1990s, for example, has coincided with worsening feeding conditions in the spring staging area in Algeria, which has increased mortality (Møller & Szép 2005b; Szép & Møller 2005). The number of breeding birds, however, depends on the size of the population after breeding the previous summer and on the number of first-year recruits. It thus depends on breeding success (e.g. Loske 1994), in particular on the proportion of fledglings from first broods, as these are more likely to recruit into the population (Møller 2002c; Chapter 9). Breeding success, particularly early in the season, thus also impacts on population size.

14639.qxd

24/1/06

202

3:54 pm

Page 202

The Barn Swallow

During the breeding season, mortality is generally not strongly related to population density in Barn Swallows (Baillie & Peach 1992). In the British population, between 1962 and 1994, survival rate, brood size and nest failure rate varied with time but not clearly with population density (Paradis et al. 2002). However, regional differences in population trends may have obscured relations with density. In Denmark, shortfalls in potential egg production during first and second clutches were positively but weakly density-dependent during the first part of Møller’s (1989a) study when the population was relatively stable in the 1970s, but not later on when it declined. That is, at higher breeding densities, clutch size tended to decrease, perhaps because of competition for nest sites and food. Chick mortality in the first brood and over the whole season was negatively density-dependent but also only weakly so. However, the frequency of infanticide has increased with increasing population density (Møller 2004a). From 1984 to 1999, the number of fledglings in Møller’s Danish population, from both first and second broods, declined, but this was offset by an increase in the percentage of pairs having second broods, so there was no overall reduction in production of fledglings (Engen et al. 2001). However, since recruits to the breeding population mainly hatch early in the year, the poor success of first broods contributed to the population decline. In a model of the dynamics of this population, Engen et al. calculated an average decrease in this population of 7.6% a year and predicted that it would go extinct within a few decades. Conditions in the winter quarters or on spring migration continue to have an effect on the breeding population (Møller 1989a). Adverse weather may both reduce numbers and leave the survivors in poor condition so that they are less able to breed successfully. Both feather growth and fat deposition may be affected (Szép & Møller 2005). If feeding conditions are good, however, poor-quality birds are likely to survive better, leading to a high level of infanticide (Møller 2004a). A study of the relation between breeding parameters in Italian Barn Swallows and the ‘normalised difference vegetation index’ (a measure of vegetation growth, Chapter 10) also found that feeding conditions in the winter quarters have consequences for the next breeding season (Saino et al. 2004c). With good winter conditions, breeding is earlier and clutch sizes larger; in addition, males have longer tails, which itself results in their mates laying more eggs (Chapter 4). As a consequence of early breeding and large clutches, fledging success is high and there are more second broods. The resulting large post-breeding population will then lead to a large breeding one the next year. Saino et al. calculated that the post-breeding population would be about 15% larger after a good winter than after a poor one. Conditions on the breeding grounds also have long-lasting effects. Investment in rearing chicks may impair the health and survival of Barn Swallows (Chapter 9) and mortality may thus be higher if poor feeding conditions force parents to work harder. Good feeding conditions are associated with increases in populations. Thus an analysis of Common Birds Census data in Scotland found that changes in Barn Swallow counts between years were positively related to changes in the abundance of insects (T. Benton, unpubl. data). This association may reflect better survival over

14639.qxd

24/1/06

Populations

3:54 pm

Page 203

203

winter for birds with abundant food in the previous summer and autumn and better survival and breeding success when migrants returning in spring also have plenty of food. The occurrence of severe cold spells in spring on the breeding grounds, and the resulting high Barn Swallow mortality (Chapter 9), may also be a factor regulating population size and in setting the northern range of the species (Brown & Brown 1999a). The impact of losses during the autumn migration on populations is less clear than for those on the winter grounds or on the spring migration. Despite large numbers of Barn Swallows dying as a result of severe weather in central Europe in October 1974, for example, there was no apparent decrease in the following year in German or Swiss populations, apart from some local declines (Bruderer 1979; Bruderer & Muff 1979). In contrast, Møller (1994a) noted that there were fewer than half as many Barn Swallows in his study area the year after. Berezovikov & Anisimov (2002) also suggested that early and persistent cold weather affecting autumn migrants might in part account for a recent decline in the Kazakhstan population. Current climate change may affect population sizes but in what direction is not clear. Early arrival and possibly later departures (Chapter 10) as a result of warmer springs and summers may lengthen the breeding season to some extent and lead to the production of more fledglings, particularly from early broods, which in turn will lead to more recruits into the breeding population the following year. Similarly, winters with high values of the North Atlantic Oscillation index (Chapter 10) lead to larger, healthier and relatively more successful first broods and hence also more breeding recruits (Møller 2002c). During the breeding season, drier conditions may reduce insect populations overall (Frampton et al. 2000) and prolonged droughts would probably reduce the breeding success of Barn Swallows; on the other hand, Barn Swallows may benefit from less rain because flying insects are more available in dry than in wet weather (Chapter 2). However, a cost to Barn Swallows in very warm conditions is that large insects may be more active and require more energy to catch. Dry weather may also make it difficult to find wet mud for nest-building. Climate change is likely to affect farming practices: with warmer, drier summers, arable farming may shift to the north and west in Britain (Robinson & Sutherland 2002), reducing ideal habitat for Barn Swallows in those areas. The effects of changes in the wintering areas are also not clear. For example, poorer feeding conditions are likely to increase mortality, lengthen the moulting period, reduce subsequent breeding success, and lead to a small population after breeding and in the following year (Saino et al. 2004a,c; Chapter 9), but an increase in savannah caused by reduced rainfall at the expense of grassland may improve foraging habitat (van Jaarsveld & Chown 2001). Droughts and a deterioration of feeding conditions along the migration route, especially in North Africa, when Barn Swallows are recovering after crossing the Sahara, would also reduce survival (Chapter 9).

14639.qxd

24/1/06

3:54 pm

204

Page 204

The Barn Swallow

Habitat change People have undoubtedly had a positive influence on Barn Swallow populations overall. When humans first became farmers about 10,000 years ago, their herds of livestock, their practice of ploughing fields and of using fire to remove scrub provided extra sources of food and their buildings offered new nest sites. More feeding and nest sites became available as agriculture spread, and people replaced woods and forests with farms, put up barns and other buildings, and constructed railways and roads with bridges and culverts. In some cases, human expansion has opened up completely new areas for Barn Swallows to nest in, in Canada and Siberia, for example. Industrialisation and even warfare have led to new types of nest sites: air raid shelters are the commonest nest sites in Orkney. In addition, Barn Swallows are generally well-liked birds and people have encouraged or at least allowed them to nest close by. Although some inconveniently sited nests are removed, many people welcome these birds, ensuring that they have access to a barn or garage. Barn Swallows and their nests were also once protected by the belief that they bring good luck and by superstitions, such as, in parts of England, that cows will give bloody milk if a Barn Swallow’s eggs are taken and, in Germany, that destroying a Barn Swallow’s nest will cause one’s house to be struck by lightning. Although farming and the growth of human communities in the past have provided an abundance of good breeding habitat for Barn Swallows, especially when the farms were small and had livestock as well as arable crops, farming practices have changed over the centuries and with them the fortunes of Barn Swallows and other farmland birds (e.g. Holloway 1996). The planting of hedgerows in Britain, especially following the Enclosure Acts of the eighteenth century, probably improved breeding habitat for Barn Swallows. In Gilbert White’s day, Barn Swallows were ‘so numerous, and so widely distributed over the village, that it is hardly possible to recount them’. In contrast, the change from mixed to arable farming in the first half of the nineteenth century probably reduced the population. During the last century, in particular, there have been dramatic changes in farming. In Britain, for example, arable farming expanded considerably after the Second World War (Robinson & Sutherland 2002). Farming became more intensive, machinery replaced horses and farms became larger but there were fewer of them. The loss of horses itself may have deprived Barn Swallows of feeding and nest sites, especially in built-up areas, but intensive farming can be disadvantageous to Barn Swallows in several other ways (Loske & Lederer 1987; Loske 1994; Evans & Robinson 2004). Most importantly, sources of flying insects are likely to be lost. Livestock are reared indoors for long periods rather than outside on pastures, land is often drained and ponds lost, grass is more frequently cut, vegetation along field borders is removed, hygiene is improved, dung heaps are replaced by slurry silos, and insects and the weeds they live on are killed with chemicals. Such intensification of farming and the loss of grazing livestock are clearly associated with reduced invertebrate numbers (e.g. Møller 2001b; Vickery et al. 2001; Benton et al. 2002; Chapter 6). On farms with livestock, anti-worming chemicals may be an

14639.qxd

24/1/06

Populations

3:54 pm

Page 205

205

additional reason for a decline in invertebrates, specifically of those feeding on dung; however, whether these affect the amount of prey available to Barn Swallows is not known (Evans & Robinson 2004). The loss of waterbodies, a preferred habitat type, may deprive Barn Swallows of both a source of insects and a source of mud for nest-building (Evans 2001). In Britain, Barn Swallows are more common in areas with cattle than in sheepgrazed or ungrazed pastures or on arable farms (Robinson et al. 2003). They prefer feeding over grazed grassland, where insects are more abundant than on silage or arable crops, and use hedgerows and waterbodies in bad weather (Chapter 2); these are good sources of insects, but are scarce on modern farms (Evans 2001; Evans & Robinson 2004). In England and Wales, the number of hedgerows declined between the mid-1940s and the early 1990s, especially in arable landscapes, while those left were often smaller and intensively managed, with gaps and fewer trees. Since the 1970s Dutch elm disease has also destroyed many hedgerow trees. Some new hedgerows have been planted, but mainly road-side ones with few plant species, which may have fewer insects. Modern farms also tend to specialise in either arable farming or livestock, instead of having a mixed system, now that farmers can use artificial fertilisers rather than manure for their crops and do not need animals for labour or their fodder crops. In Britain this has meant a concentration of arable farming, with a loss of grassland and hedgerows in eastern areas, and of livestock in the wetter west (Robinson & Sutherland 2002). This may in part explain the decline of Barn Swallows in the east and the increase in the west of Britain (Evans & Robinson 2004). Barn Swallows may concentrate in the preferred pastoral habitat in the west, and rapid intensification of arable farms may have contributed to the decline in the east (Evans 2001). Grassland management has also changed. For example, there was a decrease in the dairy herd of about 16% and an increase in sheep of over 50% between 1976 and 1997, and a rise of 100% in the use of inorganic nitrogen fertiliser on grassland between 1970 and 1986 (Vickery et al. 2001). Such changes are likely to have reduced the availability of insects and hence the suitability of farmland for Barn Swallows. Agri-environment schemes may improve the habitat for Barn Swallows, as well as for other farmland birds. Fields of cereal or oil-seed rape do provide some insects and may even be adequate in fine weather, but Barn Swallows need hedges, trees, field margins rich with flowers and insects, and a stream or pond for those occasions when the weather is bad and insects localised. Such sites are particularly important in arable areas where insects tend to be scarce anyway. Ideally, bad-weather feeding sites need to be within a couple of hundred metres of the nest site; otherwise the parents spend their time and energy travelling to and from the nest rather than collecting food. Recent reform of the EU’s Common Agricultural Policy, which decouples farming subsidies from production and links them with compliance with environmental and other standards, should benefit birds such as Barn Swallows. In England, for example, hedges are protected from cultivation and spraying; a new Environmental Stewardship Scheme also encourages environmental improvements

14639.qxd

24/1/06

206

3:54 pm

Page 206

The Barn Swallow

such as creating additional non-cultivated buffer zones along hedges. However, such measures could just be adding extras to otherwise mediocre habitat and do not address the main problem of the lack of good habitat: ideally, grazed pastures with cattle. Where good feeding sites are present but more than about 300 m from where Barn Swallows are breeding, providing extra nest sites closer to these sites may thus be another way of improving population sizes locally (K. Evans, R. Bradbury & J. Wilson, unpubl. data). Changes in land use in the winter quarters may also affect Barn Swallow populations. The felling of dense forest may create additional open habitat, but the conversion of semi-open woodland into grassland in some areas, such as West Africa, may also deprive wintering Barn Swallows of their usual foraging habitat (Evans et al. 2003b). Potentially, good foraging habitat in the winter quarters could also be reduced by more intensive farming (Evans & Robinson 2004). However, in Africa at least, fertilisers and pesticides are used at low rates and are unlikely to increase to levels comparable to those currently used in Britain. In addition, Barn Swallows feed over a wider variety of habitats and over a larger area during the non-breeding season than when breeding. Hence any reduction in insects caused by more intensive farming is likely to have little effect on Barn Swallows. Nevertheless, agricultural expansion and the reduction of wetlands in the winter quarters, especially in dry years when food is scarce anyway, may have an effect by restricting roost sites and thus potential foraging areas, and by shifting roosts to sites that are more accessible to terrestrial predators (van den Brink et al. 2000, 2003). Winter wetland roosts are also vulnerable to poisoning by avicides used against seed-eating birds, and Barn Swallows are among the non-target species killed (van den Brink & van der Have 1993; Verdoorn 1999). In addition, a succession of reedbeds or other suitable roost sites are needed along the whole migration route, not just in the winter quarters. A reduction in the availability of nest sites on farms and in villages may contribute to low breeding population densities in some areas. Studies in England, Switzerland and Germany all found a relation between population declines and a loss of nest sites (Jeromin 1999; Weggler & Widmer 2000; Evans et al. 2003c; Brombach 2004). Robinson et al. (2003) did not find such a relation, but their index of nest sites (buildings used by Barn Owls) probably excluded many sites suitable for Barn Swallows. In North America, too, declines in numbers of Barn Swallows have been attributed at least in part to the loss of nest sites on modern farms (e.g. Pennsylvania, McWilliams & Brauning 2000; Tennessee, Nicholson 1997), whereas when suitable buildings are present, pairs will nest even in large areas of monoculture (e.g. Kingery 1998). Increases in populations have sometimes been associated with increases in nest sites. In Ishikawa prefecture in Japan, over a 20-year period, population rises were associated with increases in the number of households where the Barn Swallows nested, whereas numbers fell in mountainous areas with few households (Fujita & Higuchi 1992). The increase in population in Oldisleben was also associated with the growth in horse stables (Röse 2001). Nest sites are lost for a variety of reasons, such as the abandonment of dairying, the amalgamation of small farms, the renovation of old buildings and the

14639.qxd

24/1/06

Populations

3:54 pm

Page 207

207

development of housing estates around villages. In villages, the destruction of local toilets and the securing of outbuildings against break-ins may also prevent Barn Swallows gaining access (Evans & Robinson 2004). Barn Swallows prefer to nest in traditional barns with cattle (Chapter 6). In contrast, modern buildings are sometimes unsuitable for nesting in: problems include a lack of points of access, or, with open barns, more exposure to nest predators and competitors, and fewer sites within them for nests. Buildings without livestock are also likely to be cool and less desirable for thermoregulation (Chapter 6). In North America, for example, Nicholson (1997) noted that suitable nest sites were lost when wooden barns were replaced with metal buildings, and a decline in the Czech population has also been blamed on the lack of nest sites in new barns (Kren 2000). However, not all modern buildings are unsuitable and they can provide sites for large groups (A.P. Møller, pers. comm.). Another problem on modern farms is new EU legislation currently being implemented that states that buildings used to produce or store food must be inaccessible to birds. This legislation may encourage farmers to remove Barn Swallow nests as a potential health hazard or to prevent Barn Swallows gaining access to buildings. Improved hygiene on farms will also reduce the abundance of insects close to the nest. Barn Swallows are attracted to breed at traditional sites with old nests present, and a loss of such sites is known to lead to a decline in the number of immigrants settling and thus of breeding pairs (Safran 2004). Farms and villages that lose nest sites will thus fail to attract more Barn Swallows. The loss of nest sites is clearly a factor in population declines, but is not the whole answer, however, as declines can occur when nest sites remain available (Evans et al. 2003c) and loss of nest sites sometimes just redistributes the population. Thus, in the village of Anraff, Germany, 70% of nest sites were lost between 1970 and 2000, but the Barn Swallows moved to the few buildings housing cattle and there was no population decline (Meier 2001). However, in some localities alternative nest sites may not be available and further loss of nest sites may well result in population declines. The incidence of this may increase because of the EU legislation on hygiene on farms mentioned above. In Europe, Barn Swallows are associated particularly with low-intensity livestock farms, especially those with cattle. Breeding is more successful and recruitment into the population better when livestock are present and farms with livestock may be a particularly important habitat in bad weather (Chapter 6). However, farming subsidies in the EU have resulted in a decline in the number of dairy farms, with those that remain modernising and becoming larger. Studies in Denmark and Italy have shown that Barn Swallow populations also decline when dairy farms are lost (Møller 2001b; Ambrosini et al. 2002a,b). The expansion of the EU in May 2004 may be detrimental to birds such as Barn Swallows, as there will be funds available to expand and intensify farming and for creating new infrastructure such as roads which will extend urban areas. Such projects will reduce the small-scale, low-intensity farming practices favoured by Barn Swallows. Outside the EU, in post-socialist countries, habitat may have improved for Barn Swallows in some areas, as collective farms were split into smaller units. In contrast, in Kazakhstan, farm and

14639.qxd

24/1/06

208

3:54 pm

Page 208

The Barn Swallow

village nest sites were lost when people emigrated or moved to towns, and numbers of cattle and sheep dramatically declined; this is thought to have contributed to the decline in the Barn Swallow population (Gavrilov et al. 2002). Several factors are likely to have been involved in the recent changes in Barn Swallow populations, and different factors will have affected different populations depending, for example, on where they winter and on their breeding habitat. Feeding conditions in the winter quarters or on the migration route affect survival and the timing of moult and migration and these have knock-on effects on fledging success, the proportions of second broods and of chicks recruiting into the breeding population the following year. Environmental conditions in spring, summer and autumn are also important, however, influencing breeding success and hence population sizes. Food abundance, especially early in the season at high latitudes, and nest site availability probably limit some populations, such as those in arable farmland in eastern England. However, changes in farming practices that improve the breeding habitat should allow depleted populations of Barn Swallows to recover. Regardless of conditions over winter, Barn Swallows will not thrive if, on their return, they find their nest sites gone and the fields bereft of insects.

14639.qxd

24/1/06

3:54 pm

Page 209

APPENDIX 1

Scientific names of plants and animals mentioned in the text PLANTS Elderberry Lime Maize Oak Rape Red osier dogwood

Sambucus nigra Tilia europaea Zea mays Quercus spp. Brassica napus Cornus sericea

INVERTEBRATES Antler moth Blow fly Feather lice Fire ant Louse flies Martin bug Stable fly Swallow flea Tropical fowl mite

Cerapteryx graminis e.g Protocalliphora hirundo Myrsidea rustica, Hirundoecus malleus Solenopsis invicta Stenepteryx hirundinis, Ornithomyia biloba Oeciacus hirundinis Stomoxys calcitrans Ceratophyllus hirundinis Ornithonyssus bursa

AMPHIBIANS Bullfrog

Rana catesbeiana

14639.qxd

24/1/06

3:54 pm

Page 210

210

Appendix 1

BIRDS African Hobby African River Martin American Kestrel American Robin Banded Martin Barn Owl Black Redstart Black-collared Swallow Blue Tit Boat-tailed Grackle Brazza’s Martin Brown-headed Cowbird Californian Gull Carrion Crow Cave Swallow Cliff Swallow Collared Sand Martin Common Cuckoo Common Grackle Common Magpie Common Swift Eastern Phoebe Eleonora’s Falcon Ethiopian Swallow Eurasian Blackbird Eurasian Hobby Eurasian Sparrowhawk Eurasian Tree Sparrow European Robin European Starling Gabar Goshawk Great-tailed Grackle Grey Heron Grey Kestrel Grey-rumped Swallow Horus Swift House Sparrow House Swift House Wren Lanner Falcon Large-billed Crow

Falco cuvieri Pseudochelidon eurystomina Falco sparverius Turdus migratorius Riparia cincta Tyto alba Phoenicurus ochruros Atticora melanoleuca Parus caeruleus Quiscalus major Phedina brazzae Molothrus ater Larus californicus Corvus corone Petrochelidon fulva Petrochelidon pyrrhonota Riparia riparia Cuculus canorus Quiscalus quiscula Pica pica Apus apus Sayornis phoebe Falco eleonorae Hirundo aethiopica Turdus merula Falco subbuteo Accipiter nisus Passer montanus Erithacus rubecula Sturnus vulgaris Micronisus gabar Quiscalus mexicanus Ardea cinerea Falco ardosiaceus Pseudhirundo griseopyga Apus horus Passer domesticus Apus nipalensis Troglodytes aedon Falco biarmicus Corvus macrorhynchos

14639.qxd

24/1/06

3:54 pm

Page 211

Appendix 1 Little Swift Mangrove Swallow Mascarene Martin Merlin Northern Goshawk Northern House Martin Pacific Swallow Parasitic Jaeger Peregrine Falcon Purple Martin Red-chested Goshawk Red-chested Swallow Red-necked Falcon Red-rumped Swallow Say’s Phoebe Song Thrush Spotted Flycatcher Square-tailed Saw-wing Tawny Owl Tree Swallow Welcome Swallow White-backed Swallow White-banded Swallow White-eyed River Martin White-rumped Swift White-tailed Swallow White-thighed Swallow White-throated Blue Swallow Winter Wren Yellow-billed Kite

211 Apus affinis Tachycineta albilinea Phedina borbonica Falco columbarius Accipiter gentilis Delichon urbicum Hirundo tahitica Stercorarius parasiticus Falco peregrinus Progne subis Accipiter toussenelii Hirundo lucida Falco chicquera Cecropis daurica Sayornis saya Turdus philomelos Muscicapa striata Psalidoprocne nitens Strix aluco Tachycineta bicolor Hirundo neoxena Cheramoeca leucosterna Atticora fasciata Pseudochelidon sirintarae Apus caffer Hirundo megaensis Neochelidon tibialis Hirundo nigrita Troglodytes troglodytes Milvus migrans parasitus

MAMMALS Bobcat Cat Garden Dormouse Eastern Chipmunk Raccoon Rat Red Squirrel Weasel

Lynx rufus Felis catus Elyomys quercinus Tamias striatus Procyon lotor Rattus spp. Tamiasciurus hudsonicus Mustela nivalis

14639.qxd

24/1/06

3:54 pm

Page 212

Bibliography AKOPOVA, G. V., IL’YUKH, M. P. & KHOKLOV, A. N. 2000. [Breeding Ecology of the Barn Swallow and House Martin in Stavropol Territory]. Stavropol State University [in Russian]. ALATALO, R. 1976. Haarapääskyn Hirundo rustica pesinnästä Oulussa vuosina 1966–74. Lintumies 11, 81–87. AL-RAWY, M. A. & GEORGE, P. V. 1976. Development of temperature regulation in nestling common swallows Hirundo rustica. Bulletin of the Basrah Natural History Museum 3, 77–88. AMBROSINI, R., BOLZERN, A. M., CANOVA, L., ARIENI, S., MØLLER, A. P. & SAINO, N. 2002a. The distribution and colony size of Barn Swallows in relation to agricultural land use. Journal of Applied Ecology 39, 524–534. AMBROSINI, R., BOLZERN, A. M., CANOVA, L. & SAINO, N. 2002b. Latency in response of Barn Swallow Hirundo rustica populations to changes in breeding habitat conditions. Ecology Letters 5, 640–647. ANDREW, D. G. 1993. House Martins taking over Barn Swallow’s nest. British Birds 86, 184–185. ANON. 2005. The North American Bird Information website. http://www.birdinfo.com/ BarnSwallow_bc.html ANTHONY, L. W. & ELY, C. A. 1976. Breeding biology of Barn Swallows in west-central Kansas. Kansas Ornithological Society Bulletin 27, 37–43. ARMSTRONG, E. A. 1970. The Folklore of Birds. Dover, New York. ARTEM’YEV, A. V., ZIMIN, V. B., LAPSHIN, N. V., SAZONOV, S. V., KHOKLOVA, T. Y. & YAKOVLEVA, M. V. 1993. [Ornithofauna of Karelia.] Petrozavodosk, Karelian Scientific Center, Russian Academy of Sciences [in Russian]. ASH, J. S. 1969. Spring weights of trans-Saharan migrants in Morocco. Ibis, 111 1–10. ATHERTON, P. F. 1998. Barn Swallow giving specific alarm call for Hobby. British Birds 90, 526. AYUPOV, A. S. & TAZETDINOV, M. G. 1977. [Birds of the Volga-Kama Territory]. Moscow, Nauka Press [in Russian]. BABENKO, V. G. 2000. [Birds of Lower Amur River Area]. Moscow, Promotei Press [in Russian]. BAILLIE, S. R. & PEACH, W. J. 1992. Population limitation in Palaearctic-African migrant passerines. Ibis 134, supplement 1, 120–132. BAILLIE, S. R., MARCHANT, J. H., CRICK, H. Q. P., NOBLE, D. G., BALMER, D. E., BEAVEN, L. P., COOMBES, R. H., DOWNIE, I. S., FREEMAN, S. N., JOYS, A. C., LEECH, D. I., RAVEN, M. J., ROBINSON, R. A. & THEWLIS, R. M. 2005. Breeding Birds in the wider countryside: their conservation status 2004. BTO, Thetford. http://www.bto.org/birdtrends BAIRLEIN, F. 1985. Body weights and fat deposition of Palearctic passerine migrants in the central Sahara. Oecologia 66, 141–146. BAIRLEIN, F. 1988. Herbstlicher Durchzug, Körpergewichte und Fettdeposition von Zugvögeln in einem Rastgebiet in Nordalgerien. Vogelwarte 34, 237–248.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 213

213

BAKER, R. R. 1993. The function of post-fledging exploration: a pilot study of three species of passerines ringed in Britain. Ornis Scandinavica 24, 71–79. BALL, G. F. 1982. Barn Swallow fledgling successfully elicits feeding at a non-parental nest. Wilson Bulletin, 94 362–363. BALL, G. F. 1983. Functional incubation in male Barn Swallows. Auk 100, 998–1000. BAN´ BURA, J. 1986. Sexual dimorphism in wing and tail length as shown by the swallow, Hirundo rustica. Journal of Zoology 210, 131–136. BAN´ BURA, J. & ZIELIN´ SKI, P. 1995a. A clear case of sexually selected infanticide in the swallow Hirundo rustica. Journal für Ornithologie 136, 299–301. BAN´ BURA, J. & ZIELIN´ SKI, P. 1995b. The influence of laying sequence and ambient temperature on egg size variation in the swallow Hirundo rustica. Journal für Ornithologie 136, 453–460. BAN´ BURA J. & ZIELIN´ SKI P. 1995c. The onset of incubation and hatching asynchrony in the Barn Swallow Hirundo rustica. Ornis Fennica 72, 174–176. BAN´ BURA J. & ZIELIN´ SKI P. 1998a. Timing of breeding, clutch size and double-broodedness in Barn Swallows Hirundo rustica. Ornis Fennica 75, 177–183. BAN´ BURA, J. & ZIELIN´ SKI, P. 1998b. An analysis of egg-size repeatability in Barn Swallows Hirundo rustica. Ardeola 45, 183–192. BAN´ BURA, J. & ZIELIN´ SKI, P. 2000. Repeatability of reproductive traits in female Barn Swallows Hirundo rustica. Ardea 88, 75–80. BANSEMER, H. 2001. Schizochroistische Rauchschwalben Hirundo rustica. Ornithologische Mitteilungen 53, 385–387. BARBOSA, A. & MØLLER, A. P. 1999a. Sexual selection and tail streamers in the Barn Swallow: appropriate tests of the function of size-dimorphic long tails. Behavioral Ecology 10, 112–114. BARBOSA, A. & MØLLER, A. P. 1999b. Aerodynamic costs of long tails in male Barn Swallows Hirundo rustica and the evolution of sexual size dimorphism. Behavioral Ecology 10, 128–135. BARBOSA, A., MERINO, S., DE LOPE, F. & MØLLER, A. P. 2002. Effects of feather lice on flight behavior of male Barn Swallows (Hirundo rustica). Auk 119, 213–216. BARBOSA, A., MERINO, S., CUERVO, J.J., DE LOPE, F. & MØLLER, A. P. 2003. Feather damage of long tails in Barn Swallows Hirundo rustica. Ardea, 91, 85–90. BARCLAY, R. M. R. 1988. Variation in the costs, benefits, and frequency of nest reuse by Barn Swallows (Hirundo rustica). Auk 105, 53–60. BARRENTINE, C. D. 1980. The ingestion of grit by nestling Barn Swallows. Journal of Field Ornithology 1, 368–371. BAUER, H. G. & HEINE, G. 1992. Die Entwicklung der Brutvolgelbestande am Bodensee: Vergleich halbquantitativer Rasterteartierungen 1980/81 und 1990/91. Journal für Ornithologie 133, 1–22. BAXTER, E. V. & RINTOUL, L. J. 1953. The Birds of Scotland. Their History, Distribution and Migration. Volume 1. Oliver & Boyd, Edinburgh. BEAL, F. E. L. 1918. Food habits of the swallows, a family of valuable native birds. Bulletin of the United States Department of Agriculture 619, 1–28. BEECHER, M. D., MEDVIN, M. B., STODDARD, P. K. & LOESCHE, P. 1986. Acoustic adaptations for parent-offspring recognition in swallows. Experimental Biology 45, 179–193. BEENEN, H. 1970. Bestandsaufnahme der Rauch und Mehlschwalbe in Solingen-Ohligs in Jahren 1966–1968. Charadrius 6, 90–91.

14639.qxd

24/1/06

214

3:54 pm

Page 214

Bibliography

BEESTON, H. 1907. Observations of an attempt of the swallow tribe to winter in south Hants during 1906–7. The Zoologist 227–234, 267–271, 303–306. BENT, A. C. 1942. Life Histories of North American Flycatchers, Larks, Swallows, and their Allies. Dover Press, New York. BENTON, T. G., BRYANT, D. M., COLE, L. & CRICK, H. Q. P. 2002. Linking agricultural practice to insect and bird populations: a historical study over three decades. Journal of Applied Ecology 39, 673–687. BEREZOVIKOV, N. N. & ANISIMOV, E. I. 2002. [Mass mortality of Barn Swallows Hirundo rustica in the autumn of 2000 in the Alakol Depression.] Russian Journal of Ornithology 11, 258–261 [in Russian]. BERGMANN, H. H. & HELB, H. W. 1982. Stimmen der Vögel Europas: Gesange und Rufe von uber Vogelarten in mehr als Sonogrammen. BLV, Munich. BERNDT, R. & BERNDT, A. 1942. Beobachtungen uber das Brutgeschaften eines RauchschwalbenPaares. Beiträge Fortpflanzen de Vogel 18, 130–134. BERTHOLD, P. 2001. Bird Migration. Second edition. Oxford University Press, Oxford. BERTHOLD, P. 2003. Changes in the breeding bird fauna of two southern German rural communities during recent decades: lost paradises? Journal für Ornithologie 144, 385–410. BIEBACH, H. 1992. Flight-range estimates for small trans-Sahara migrants. Ibis 134. supplement 1, 47–54. BIEBACH, H., FRIEDRICH, W., HEINE, G., JENNI, G., JENNI-EIERMANN, S. & SCHMIDT, D. 1991. The daily pattern of autumn bird migration in the northern Sahara. Ibis 133, 414–422. BIJLSMA, R. G. & VAN DEN BRINK, B. In press. A Barn Swallow Hirundo rustica roost under attack: timing and risks in the presence of African Hobbies Falco cuvieri. Ardea. BIRDLIFE INTERNATIONAL 2000. Threatened Birds of the World. BirdLife International, Cambridge. BIRDLIFE INTERNATIONAL 2004. Species factsheet: Hirundo rustica. http://www.birdlife.org. BIRKHEAD, T. R. & MØLLER, A. P. 1992. Sperm Competition in Birds: Evolutionary Causes and Consequences. Academic Press, London. BLACKWELL, A. 1997. Diel flight periodicity of the biting midge Culicoides impunctatus and the effects of meteorological conditions. Medical and Veterinary Entomology 11, 361–367. BLAKE, R. W., KOLOTYLO, R. & DE LA CUEVA, H. 1990. Flight speeds of the Barn Swallow, Hirundo rustica. Canadian Journal of Zoology 68, 1–5. BLEM, C. R. & BLEM, L. B. 1992. Some observations of sunbathing in swallows. Journal of Field Ornithology 63, 53–56. BLEM, C. R. & BLEM, L. B. 1993. Do swallows sunbathe to control ectoparasites? An experimental test. Condor 95, 728–730. BÖHNING-GAESE, K. & BAUER, H-G. 1996. Changes in species abundance, distribution, and diversity in a Central European bird community. Conservation Biology 10, 175–187. BOYD, A. W. 1935. Report on the swallow enquiry, 1934. British Birds 29, 3–21. BOYD, A. W. 1936. Report on the swallow enquiry, 1935. British Birds 30, 98–116. BOYLE, G. 1995. Swallows roosting on ship at night. British Birds 85, 616–617. BOWDEN, S. 2005. Common Cuckoo parasitising Barn Swallow. British Birds 98, 607. BRAZIL, M. P. 1991. The Birds of Japan. Christopher Helm, London. BREWER, R., PEEK, G. A. M. & ADAMS, Jr, R. L. 1991. The Atlas of Breeding Birds of Michigan. Michigan State University Press, East Lansing.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 215

215

BRICENO, A. T. 2002. Tail Length and Sexual Selection in the North American Barn Swallow Hirundo rustica erythrogaster. MS thesis, University of Tulsa. BRICHETTI, P. & CAFFI, M. 1992. Biologia reproduttiva di una popolazione di rondine, Hirundo rustica, nidificante in un cascinale della Padania (Aves, Hirundinidae). Rivista Piemontese di Storia Naturale 13, 73–87. BROEKHUYSEN, G. J. 1952. Hirundo rustica feeding on amphipoda. Ostrich 23, 134–135. BROEKHUYSEN, G. J. 1953. A post mortem of the Hirundinidae which perished at Somerset West in April 1953. Ostrich 24, 148–152. BROEKHUYSEN, G. J. 1964. The status and movements of the European Swallow, Hirundo rustica, in the most southern part of Africa. Ardea 52, 140–165. BROEKHUYSEN, G. J. & BROWN, A. R. 1963. The moulting pattern of European Swallows, Hirundo rustica, wintering in the surroundings of Cape Town, South Africa. Ardea 51, 25–43. BROMBACH, H. 2004. Die Rauchschwalbe. Westarp Wissenschaftlen, Hohenwarsleben. BROOKE, R. K. 1956. Food of the European swallow. Ostrich 27, 88. BROOKE, R. K. 1995. An examination of road-killed European Swallow Hirundo rustica moults. Safring News 24, 42. BROWN, C. R. 1985. Vocalizations of barn and cliff swallows. Southwestern Naturalist 30, 325–333. BROWN, C. R. & BROWN, M. B. 1996. Coloniality in the Cliff Swallow: the Effect of Group Size on Social Behavior. University of Chicago Press, Chicago. BROWN, C. R. & BROWN, M. B. 1999a. Barn Swallow (Hirundo rustica). In Poole, A. & Gill, F. (eds), The Birds of North America, No. 452. The Birds of North America, Inc., Philadelphia, PA. BROWN, C. R. & BROWN, M. B. 1999b. Natural selection on tail and bill morphology in Barn Swallows Hirundo rustica during severe weather. Ibis 141, 652–659. BROWN, C. R. & BROWN, M. B. 1999c. The evolution of coloniality: the importance of colony size. In Adams, N. J. & Slotow, R. H. (eds), Proceedings of the 22nd International Ornithological Congress, Durban, pp. 1293–1303. BirdLife International, Johannesburg. BROWN, C. R. & HOOGLAND, J. L. 1986. Risk in mobbing for solitary and colonial swallows. Animal Behaviour 34, 1319–1323. BROWN, C. R. & RANNALA, B. 1995. Colony choice in birds: models based on temporally invariant site quality. Behavioral Ecology and Sociobiology 36, 221–228. BROWN, C. R. & SHERMAN, L. C. 1989. Variation in the appearance of swallow eggs and the detection of intraspecific brood parasitism. Condor 91, 620–627. BRUDERER, B. 1979. Zum Zahreszyklus schweizerischer Schwalben (Hirundo rustica und Delichon urbica) unter besonderer Berücksichtigung des Katastrophenjahres 1974. Ornithologische Beobachter 76, 293–304. BRUDERER, B. & BOLDT, A. 2001. Flight characteristics of birds: 1. Radar measurements of speed. Ibis 143, 178–204. BRUDERER, B. & MUFF, J. 1979. Bestandesschwankungen schweizerischer Rauch-und Mehlschwalben, insbesondere im Zusammenhang mit der Schwalbenkatastrophe im Herbst 1974. Ornithologische Beobachter 76, 229–234. BRUDERER, L., LIECHTI, F. & BILO, D. 2001. Flexibility in flight behaviour of Barn Swallows (Hirundo rustica) and House Martins(Delichon urbica) tested in a wind tunnel. Journal of Experimental Biology 204, 1473–1484.

14639.qxd

24/1/06

216

3:54 pm

Page 216

Bibliography

BRYANT, D. M. 1975. Breeding biology of the House Martin, Delichon urbica, in relation to aerial insect abundance. Ibis 117, 180–215. BRYANT, D. M. & TURNER, A. K. 1982. Central place foraging by swallows (Hirundinidae): the question of load size. Animal Behaviour 30, 845–856. BRYANT, D. M. & WESTERTERP, K. R. 1983. Short-term variability in energy turnover by breeding House Martins Delichon urbica: a study using doubly labelled water D218O. Journal of Animal Ecology 52, 522–543. BUCHANAN, K. L. & EVANS, M. R. 2000. The effect of tail streamer length on aerodynamic performance in the Barn Swallow. Behavioral Ecology 11, 228–238. BUCHANAN, K. L. & EVANS, M. R. 2001. Flight, fitness and sexual selection: a response. Behavioral Ecology 12, 513–515. BUCKLAND, S. T., BELL, M. V. & PICOZZI, N. 1990. The Birds of North-East Scotland. North-East Scotland Bird Club, Aberdeen. BULGARINI, F. & VISENTIN, M. 1997. Nocturnal feeding by Barn Swallows and House Martins. British Birds 90, 363. BURLEY, N. 1986. Sexual selection for aesthetic traits in species with biparental care. American Naturalist 127, 415–445. BURTON, J. F. 1994. Barn Swallow trapped by greater burdock. British Birds 87, 144. BURTT, E. H. Jr. 1977. Some factors in the timing of parent-chick recognition in swallows. Animal Behaviour 25, 231–239. BURTT, E. H. Jr, BITTERBAUM, E. J. & HAILMAN, J. P. 1988. Head-scratching method in swallows depends on behavioral context. Wilson Bulletin 100, 679–682. BUTLER, C. J. 2003. The disproportionate effect of global warming on the arrival dates of shortdistance migratory birds in North America. Ibis 145, 484–495. BUTLER, R. W. & CAMPBELL, C. A. 1987. Nest appropriation and interspecific feeding between Tree Swallows, Tachycineta bicolor, and Barn Swallows, Hirundo rustica. Canadian Field-Naturalist 101, 433–434. BUTTERFIELD, D. P. & RAMSAY, A. D. K. 1998. Breeding biology of Swallows in Easter Ross. Scottish Birds 19, 141–144. CABELLO DE ALBA, F. 2002. Lower reproductive success in Barn Swallows Hirundo rustica after massive aerial treatment with Bacillus thuringiensis. Ardeola 49, 91–95. CADÉE, N. 2000. Parent Barn Swallow fluctuating asymmetry and offspring quality. Journal of Avian Biology 31, 495–503. CAMPLANI, A., SAINO, N. & MØLLER, A. P. 1999 Carotenoids, sexual signals and immune function in Barn Swallows from Chernobyl. Proceedings of the Royal Society of London B 266, 1111–1116. CANNELL, M. G. R., PALUTIKOF, J. P. & SPARKS, T. H. (eds) 1999. Indicators of Climate Change in the UK. Department of Environment, Transport and Regions, London. CHRISTENSEN, P. 1981. Recoveries of Danish swallows Hirundo rustica in Denmark. Dansk Ornitologisk Forenings Tidsskrift 75, 47–50. COAN, D. R. 1990. Swallows destroying House Martin’s nests. British Birds 83, 24. CONOLE, L. E. & BAVERSTOCK, G. A. 1994. Possible hybrid swallow Hirundo neoxena x rustica in Victoria. Bird Observer 739, 15. CRAMP, S. (ed.) 1980. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Volume 2. Oxford University Press, Oxford.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 217

217

CRAMP, S. (ed.) 1988. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Volume 5. Oxford University Press, Oxford. CRICK, H. Q. P. & SPARKS, T. H. 1999. Climate change related to egg-laying trends. Nature 399, 423–424. CRICK, H. Q. P., BAILLIE, S. R. & LEECH, D. I. 2003. The UK Nest Record Scheme: its value for science and conservation. Bird Study 50, 254–270. CROOK, J. R. & SHIELDS, W. M. 1985. Sexually selected infanticide by adult male Barn Swallows. Animal Behaviour 33, 754–761. CROOK, J. R. & SHIELDS, W. M. 1987. Non-parental nest attendance in the Barn Swallow (Hirundo rustica): helping or harassment? Animal Behaviour 35, 991–1001. CUERVO, J. J. 2000. Foraging cost of ornaments which are not ornaments: comment on Matyjasiak et al. 1999. Ethology 106, 659–663. CUERVO, J. J. & DE AYALA, R. M. In press. Experimental tail shortening in Barn Swallows Hirundo rustica affects haematocrit. Functional Ecology. CUERVO, J. J., DE LOPE, F., MØLLER, A. P. & MORENO, J. 1996a. Energetic cost of tail streamers in the Barn Swallow (Hirundo rustica). Oecologia 108, 252–258. CUERVO, J. J., DE LOPE, F. & MØLLER, A. P. 1996b. The function of long tails in female Barn Swallows (Hirundo rustica): an experimental study. Behavioral Ecology 7, 132–136. CUERVO, J. J., MØLLER, A. P. & DE LOPE, F. 2003. Experimental manipulation of tail length in female Barn Swallows (Hirundo rustica) affects their future reproductive success. Behavioral Ecology 14, 451–456. CURRY-LINDAHL, K. 1953. Tropiska Fjäll. Stockholm. DANCHIN, E., BOULINIER, T. & MASSOT, M. 1998. Conspecific reproductive success and breeding habitat selection: implications for the study of coloniality. Ecology 79, 2415–2428. DANIELSEN, R. 1988. Bounding flight in passerines: some empirical data. Dansk Ornitologisk Forenings Tidsskrift 82, 59–60. DANILOV, N. N., RYZHANOVSKIY, V. N. & RYABITSEV, V. K. 1984. [Birds of Yamal Peninsula.] Moscow, Nauka Press [in Russian]. DAWKINS, R. & CARLISLE, T. R. 1976. Parental investment, mate desertion and a fallacy. Nature 262, 131–133. DE LA CUEVA, H., & BLAKE, R. W. 1997. Flight speed, foraging efficiency, and daily energy budget of the Barn Swallow, Hirundo rustica. Canadian Journal of Zoology 75, 1176–1183. DE LOPE, F. 1985. Pterilosis y dimorfismo sexual de Hirundo rustica L. en Extremadura (España). Ardeola 32, 3–8. DE LOPE, F. & DE LA CRUZ, C. 1989. El desarrollo de los pollos en la golondrina común Hirundo rustica L.: las diferencias entre las crianzas. Ardeola 36, 55–60. DE LOPE, F. & MØLLER, A. P. 1993a. Effects of ectoparasites on reproduction of their swallow hosts: a cost of being multi-brooded. Oikos 67, 557–562. DE LOPE, F. & MØLLER, A. P. 1993b. Female reproductive effort depends on the degree of ornamentation of their mates. Evolution 47, 1152–1160. DE LOPE REBOLLO, F. 1983. La reproduction d’Hirundo rustica en Estremadure (Espagne). Alauda 51, 81–91. DHONDT, A. A. E. & HOCHACHKA, W. M. 2001. Variations in calcium use by birds during the breeding season. Condor 103, 592–598.

14639.qxd

24/1/06

218

3:54 pm

Page 218

Bibliography

DICKINSON, E. C. & DEKKER, R. W. R. J. 2001. Systematic notes on Asian birds. 13. A preliminary review of the Hirundinidae. Zoologische Verhandelingen Leiden 335, 127–144. DICKINSON, E. C., ECK, S. & MILENSKY, C. M. 2002. Systematic notes on Asian birds. 31. Eastern races of the Barn Swallow Hirundo rustica Linnaeus, 1758. Zoologische Verhandelingen Leiden 335, 145–166. DIMARCA, A. & LO VALVO, M. 1987. Dati sulla biologia riproduttiva della rondine, Hirundo rustica, in Sicilia. Rivista Italiana di Ornitologia Milano 57, 85–96. DOBSON, A. P. 1987. A comparison of seasonal and annual mortality for both sexes of fifteen species of common British birds. Ornis Scandinavica 18, 122–128. DOWSETT, R. J. 1966. The moulting pattern of European swallows, Hirundo rustica, wintering in Eastern Zambia. Puku 4, 91–100. DRAGUNKINA, N. S. 1986. [The Study of the Birds of the USSR, their Conservation and Wise Management.]. Volume. 1. Leningrad [in Russian]. DRENT, R. 1975. Incubation. In Farner, D.S. & King, J.R. (eds), Avian Biology, pp. 333–420. Academic Press, New York. DUBOWY P. J. & MOORE, S. W. 1985. Weather-related mortality in swallows in the Sacramento Valley of California. Western Birds 16, 49–50. DUFFIN, K. 1973. Barn Swallows use freshwater and marine algae in nest construction. Wilson Bulletin 85, 237–238. EARLÉ, R. A. 1997. European Swallow Hirundo rustica. In Harrison, J. A., Allan, D. G., Underhill, L. G., Herremans, M., Tree, A. J., Parker, V. & Brown, C. J. (eds), The Atlas of Southern African Birds.. Volume 2. Passerines, pp. 48–49. BirdLife South Africa, Johannesburg. EGGER, B. 2000. Foraging Performance of Barn Swallows Hirundo rustica in Relation to Food Supply and Consequences for Nestling Growth and Survival. Diploma thesis, University of Bern and Swiss Ornithological Institute, Sempach. ELLEGREN, H. 1993. Speed of migration and migratory flight lengths of passerine birds ringed during autumn migration in Sweden. Ornis Scandinavica 24, 220–228. ELLEGREN, H., LINDGREN, G., PRIMMER, C. R. & MØLLER, A. P. 1997. Fitness loss and germline mutations in Barn Swallows breeding in Chernobyl. Nature 389, 593–596. ENGEN, S., SAETHER, B-E. & MØLLER, A. P. 2001. Stochastic population dynamics and time to extinction of a declining population of swallows. Journal of Animal Ecology 70, 789–797. ENGSTRAND, S. M. & BRYANT, D. M. 2002. A trade-off between clutch size and incubation efficiency in the Barn Swallow Hirundo rustica. Functional Ecology 16, 782–791. ERRITZOE, J., MAZGAJSKI, T. D. & REJT, L. 2003. Bird casualties on European roads: a review. Acta Ornithologica 38, 77–93. ERSKINE, A. J. 1979. Man’s influence on potential nesting sites and populations of swallows in Canada. Canadian Field-Naturalist 93, 371–377. EVANS, K. L. 2001. The Effects of Agriculture on Swallows Hirundo rustica. D.Phil. thesis, University of Oxford. EVANS, K. L. & ROBINSON, R. A. 2004. Barn Swallows and agriculture. British Birds 97, 218–230. EVANS, K. L., BRADBURY, R. B. & WILSON, J. D. 2003a. Selection of hedgerows by swallows Hirundo rustica foraging on farmland: the influence of local habitat and weather. Bird Study 50, 8–14. EVANS, K. L., WALDRON, S. & BRADBURY, R. B. 2003b. Segregation in the African wintering ranges of English and Swiss swallow Hirundo rustica populations: a stable isotope study. Bird Study 50, 294–299.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 219

219

EVANS, K. L., WILSON, J. D. & BRADBURY, R. B. 2003c. Swallow Hirundo rustica population trends in England: data from repeated historical surveys. Bird Study 50, 178–181. EVANS, M. R. 1998. Selection on swallow tail streamers. Nature 394, 233–234. EVANS, M. R. 2003. Birds’ tails do act like delta wings but delta-wing theory does not always predict the forces they generate. Proceedings of the Royal Society of London B 270, 1379–1385. EVANS, M. R. 2004. Limits on the evolution of tail ornamentation in birds. American Naturalist 163, 341–357. EVANS, M. R. & THOMAS, A. L. R. 1997. Testing the functional significance of tail streamers. Proceedings of the Royal Society of London B 264, 211–217. EVANS, M. R., MARTINS, T. L. F. & HALEY, M. 1994. The asymmetrical cost of tail elongation in red-billed streamer-tails. Proceedings of the Royal Society of London B 256, 97–103. EVANS, M. R., ROSÉN, M., PARK, K. L. & HEDENSTRÖM, A. 2002. How do birds’ tails work? Deltawing theory fails to predict tail shape during flight. Proceedings of the Royal Society of London B 269, 1053–1057. EVANS, T. D., WATSON, L. G. & DUCKWORTH, J. W. 2000. Large-scale swallow trapping in Xiangkhouang Province, North Laos. Oriental Bird Club Bulletin 32, 59–62. EWINS, P .J., ROUND, P. D. & BAZELY, D. R. 1991. Urban roosting by Barn Swallows Hirundo rustica wintering in Thailand. Forktail 6, 68–70. FENECH, N. 1992. Fatal Flight. The Maltese Obsession with Killing Birds. Quiller Press. FERRO, G. & BOANO, G. 1998. Sopravvivenza e filopatria della rondine Hirundo rustica in Italia settentrionale. Avocetta 22, 27–34. FINLAYSON, C. 1992. Birds of the Strait of Gibraltar. T. & A D Poyser, London. FLORIDA FISH AND WILDLIFE CONSERVATION COMMISION. 2003. Florida’s breeding bird atlas: A collaborative study of Florida’s birdlife. http://www.wildflorida.org/bba/ FLUMM, D. S. 1975. Aberrant or hybrid swallow. British Birds 68, 246–247. FOLSTAD, I. & KARTER, J. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622. FORCHHAMMER, M. C., POST, E. & STENSETH, N. C. 2002. North Atlantic Oscillation timing of long- and short-distance migration. Journal of Animal Ecology 71, 1002–1014. FORD, A. A. & ELPHICK, D. 1993. Barn Swallows roosting in maize. British Birds 86, 95–96. FORSTER, T. 1817. Observations of the Natural History of Swallows with a Collateral Statement of Facts Relative to their Migration and to their Brumal Torpidity. Sixth edition. Reproduction 1972, Redwood Press, London. FOSSI, M. C., MASSI, A. & LEONZIO, C. 1994. Blood esterase inhibition in birds as an index of organophosphorus contamination: field and laboratory studies. Ecotoxicology 3, 11–20. FRAMPTON, G. K., VAN DEN BRINK, P. J. & GOULD, P. J. L. 2000. Effects of spring drought and irrigation on farmland arthropods in southern Britain. Journal of Applied Ecology 37, 865–883. FUJITA, G. & HIGUCHI, H. 1992. The relationship between habitat changes and population dynamics in Barn Swallows. Strix 11, 169–177. GABRIEL, K. R. 1975. Swallows feeding wasps to young. British Birds 68, 248. GALEOTTI, P., SAINO, N., SACCHI, R. & MØLLER, A. P. 1997. Song correlates with social context, testosterone and body condition in male Barn Swallows. Animal Behaviour 53, 687–700. GALEOTTI, P., SAINO, N., PERANI, E., SACCHI, R. & MØLLER, A. P. 2001. Age-related song variation in male Barn Swallows. Italian Journal of Zoology 68, 305–310.

14639.qxd

24/1/06

220

3:54 pm

Page 220

Bibliography

GARAMSZEGI, L. Z., HEYLEN, D., MØLLER, A. P., EENS, M. & DE LOPE, F. 2005. Age-dependent health status and song characteristics in the Barn Swallow. Behavioral Ecology 16, 580–591. GATTER, V. W. & BEHRNDT, M. 1985. Unterschiedliche tageszeitliche Zugmuster alter und junger Vogel am Beispiel der Rauchschwalbe Hirundo rustica. Vogelwarte 33, 115–120. GAVRILOV, E. I., GRACHEV, U. N., NILOV, V. I., BRAGIN, B. I. & BIRDZANOVA, N. H. 1994. [Experiment on comparative estimations of environmental pollution by organochlorine pesticides and heavy metals in Asia and Africa.] Selevinia, 4, 52–55 [in Russian]. GAVRILOV, E. I., GAVRILOV, A. E. & KOVSHAR, V. A. 2002. Long-term fluctuations in numbers of swallows Hirundo rustica on seasonal migration in the foothills of West Tien Shan South Kazakhstan. Avian Ecology and Behaviour 8, 1–22. GEORGE, P. V. 1965. Swallows Hirundo rustica Linnaeus roosting on wires. Journal of the Bombay Natural History Society 62, 160. GEORGE, P. V. 1976. Hirundo rustica moulting remiges while rearing nestlings in Iraq. Bulletin of the Basrah Natural History Museum 3, 95–100. GEORGE, P. V. & AL-RAWY, M. 1970. Growth studies on nestlings of common swallow Hirundo rustica rustica. Bulletin of the Iraqi Natural History Museum 4, 3–20. GÉROUDET, P. 1961. La Vie des Oiseaux. Les Passereaux 1. Delachaux et Niestlé, Neuchâtel. GIBBONS, D. W., REID, J. B. & CHAPMAN, R. A. 1993. The New Atlas of Breeding Birds in Britain and Ireland: 1988–91. T & A D Poyser, London. GIBBONS, D. W., AVERY, M. I. & BROWN, A. F. 1996. Population trends of breeding birds in the United Kingdom since 1800. British Birds 89, 291–305. GIL, D. & GAHR, M. 2002. The honesty of bird song: multiple constraints for multiple traits. Trends in Ecology and Evolution 17, 133–141. GIL, D., NINNI, P., LACROIX, A., DE LOPE, F., TIRARD, C., MARZAL, A. & MØLLER, A. P. 2005. Yolk androgens in the Barn Swallow Hirundo rustica: a test of some adaptive hypotheses. Journal of Evolutionary Biology. GIUNCHI, D. & BALDACCINI, N. E. 2004. Orientation of juvenile Barn Swallows (Hirundo rustica) tested in Emlen funnels during autumn migration. Behavioral Ecology and Sociobiology 56, 124–131. GLADSTONE, H. S. 1910. The Birds of Dumfriesshire. London, Witherby. GLOWACKI, J. 1977. [Contribution to the knowledge of the composition of the diet of swallows (Hirundo rustica L.)] Przeglad Zoologiczny 21, 60–61 [in Russian]. GLUE, D. 1994. Juvenile migrant Barn Swallows in Britain in 1991. British Birds 87, 625. GLUTZ VON BLOTZHEIM, U. N. & BAUER, K. M. 1985. Handbuch der Vögel Mitteleuropas. Volume 10. AULA-Verlag, Wiesbaden. GOODMAN, S. M. 1982. A test of nest cup volume and reproductive success in the Barn Swallow. Jack-Pine Warbler 60, 107–112. GOODMAN, S. M. & MEININGER, P. L. 1989. The Birds of Egypt. Oxford University Press, Oxford. GOODWIN, T. W. 1984. The Biochemistry of the Carotenoids. II. Animals. Chapman & Hall, London. GORDO, O., BROTONS, L., FERRER, X. & COMAS, P. 2005. Do changes in climate patterns in wintering areas affect the timing of the spring arrival of trans-Saharan migrant birds? Global Change Biology 11, 12–21. GOSSIP, P. W. 1995. Swallows mobbing Grey Heron. Scottish Bird News 39, 6. GRAFEN, A. 1990. Sexual selection unhandicapped by the Fisher process. Journal of Theoretical Biology 144, 517–546.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 221

221

GREENWOOD, P. J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28, 1140–1162. GREGORY, G., ROBERTSON, P. & THOMAS, B. 2001. Reduction of bird shooting in Kuwait. Sandgrouse 23, 34–38. GRIFFITH, S. C., LYON, B. E. & MONTGOMERIE, R. 2004. Quasi-parasitism in birds. Behavioral Ecology and Sociobiology 56, 191–200. GRIMMETT, R., INSKIPP, C. & INSKIPP, T. 1998. Birds of the Indian Subcontinent. A&C Black, London. GROBLER, G. P. J. & NUTTALL, R. J. 1999. Interesting European Swallow behaviour. Mirafra 16, 17. GRUE, C. E., O’SHEA, T. J. & HOFFMAN, D. J. 1984. Lead concentrations and reproduction in highway-nesting Barn Swallows. Condor 86, 383–398. GRÜEBLER, M. & NAEF-DAENZER, B. 2003. To feed or not to feed? A trade-off in the postfledging parental care in the double-brooded Barn Swallow Hirundo rustica. Vogelwarte 42, 103–104. GRZYBOWSKI, J. A. 1979. Responses of Barn Swallows to eggs, young, nests and nest sites. Condor 81, 236–246. GUERRIERI, G., BIONDI, M. & PIETRELLI, L. 1990. Influenza di parametri meteorologici ed ambientali sullo svernamento della rondine Hirundo rustica, nell’Italia centrale. Rivista Italiana di Ornitologia Milano 60, 137–146. HAFTORN, S. 1988. Incubating female passerines do not let the egg temperature fall below the ‘physiological zero temperature’ during their absences from the nest. Ornis Scandinavica 19, 97–110. HAILS, C. J. 1979. A comparison of flight energetics in hirundines and other birds. Comparative Biochemistry and Physiology 63A, 581–585. HAILS, C. J. 1983. A comparison of tropical and temperate aerial insect abundance. Biotropica 14, 310–313. HAMILTON, W. D. & ZUK, M. 1982. Heritable true fitness and bright birds: a role for parasites. Science 218, 384–387. HANSELL, M. 2000. Bird Nests and Construction Behaviour. Cambridge University Press, Cambridge. HAYWOOD, S. 1993. Sensory and hormonal control of clutch size in birds. Quarterly Review of Biology 68, 33–60. HEBBLETHWAITE, M. L. & SHIELDS, W. M. 1990. Social influences on Barn Swallow foraging in the Adirondacks: a test of competing hypotheses. Animal Behaviour 39, 97–104. HEDENSTRÖM, A. 1995. Swallows unhandicapped by long tails? Trends in Ecology and Evolution 10, 140–141. HEDENSTRÖM, A. 2002. Aerodynamics, evolution and ecology of avian flight. Trends in Ecology and Evolution 17, 415–422. HENEBERG, P. 1997. [The first occurrence of the hybrid Hirundo rustica and Riparia riparia in North Bohemia]. Sbornik Severoceskeho Musea Prirodni Vedy Scientiae Naturales 20, 99–100 [in Czech]. HILLGARTH, N. & WINGFIELD, J. C. 1997. Parasite-mediated sexual selection: endocrine aspects. In Clayton, D. H. & Moore, J. (eds), Host-Parasite Evolution. General Principles and Avian Models, pp. 78–104. Oxford University Press, Oxford. HOERNECKE, E. 1990. Weitere Nachweise albinotischer Rauchschwalben Hirundo rustica. Charadrius 26, 289–290. HOFMEYR, J. 1989. European swallows feeding on rooikrans. Promerops 187, 15–17. HOLLOWAY, S. 1996. The Historical Atlas of Breeding Birds in Britain and Ireland 1875–1900. T & A D Poyser, London.

14639.qxd

24/1/06

222

3:54 pm

Page 222

Bibliography

HOLMES, A. S. 1978. Swallow hawking insects at 04.00 hours. British Birds 71, 47. HOLROYD, G. L. 1975. Nest site availability as a factor limiting population size of swallows. Canadian Field-Naturalist 89, 60–64. HÖLZINGER, J. 1969. Fünfjährige Untersuchungen über den Brutbestand der Mehl- und Rauchschwalbe (Delichon urbica et Hirundo rustica) in der Umgebung von Ulm. Anzeiger der Ornithologischen Gesellschafts Bayern 8, 610–624. HOSKING, E. & NEWBERRY, C. 1946. The Swallow. Collins, London. HOUSTON, A. 1985. Central-place foraging: some aspects of prey choice for multiple-prey loaders. American Naturalist 125, 811–826. HUBALEK, Z. 2003. Spring migration of birds in relation to North Atlantic Oscillation. Folia Zoologica 52, 287–298. HUBALEK-ZDENEK, A. 1997. Trends of bird populations in a managed lowland riverine ecosystem. Folia Zoologica 46, 289–302. HUIN, N. & SPARKS, T. H. 1998. Arrival and progression of the Swallow Hirundo rustica through Britain. Bird Study 45, 361–370. HUNT, S., KILNER, R. M., LANGMORE, N. E. & BENNETT, A. T. D. 2003. Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proceedings of the Royal Society of London B 270, S25–S28. HÜPPOP, O. & HÜPPOP, K. 2003. North Atlantic Oscillation and timing of spring migration in birds. Proceedings of the Royal Society of London B 270, 233–240. HURRELL, J. W., KUSHNIR, Y. & VISBECK, M. 2001. The North Atlantic Oscillation. Science 291, 603–605. HUTTON, A. E. 1978. Spatial relationships in perching barn and cliff swallows. Wilson Bulletin 90, 396–403. ISENMANN, P. 1999. Hirondelles de fenêtre et rustique en altitude en Savoie. Alauda 67, 71–72. IVERSON, S. S. 1988. Site tenacity in culvert-nesting Barn Swallows in Oklahoma. Journal of Field Ornithology 59, 337–344. IWASA, Y., POMIANKOWSKI, A. & NEE, S. 1991. The evolution of costly mate preferences. II. The ‘handicap’ principle. Evolution 45, 1431–1442. JACKSON, J. A. & BURCHFIELD, P .G. 1975. Nest site selection of Barn Swallows in East Central Mississippi. American Midland Naturalist 94, 503–509. JACOB, J-P. 1998. Des hirondelles de cheminée Hirundo rustica se nourissant sur un tas de fumier. Aves 35, 125. JARRY, G. 1980. Dynamique d’une population d’Hirondelles rustiques, Hirundo rustica L., dans l’est de la région parisienne. L’Oiseau et R.F.O. 50, 277–294. JARRY, G. 1987. Caractéristiques de la philopatrie chez l’hirondelle de cheminée Hirundo rustica en Seine-et-Marne. Alauda 55, 295–298. JENNER, E. W. C. 1945. Swallows of first brood assisting parents to build second nest and feed second brood. British Birds 38, 237. JENNI, L. & WINKLER, R. 1994. Moult and Ageing of European Passerines. Academic Press, London. JEROMIN, K. 1999. Die Brutvogel des Dorfes Labenz 1931 und 1995: Wandel von Dorfstruktur und Vogelwelt. Corax 18, 88–103. JONES, G. 1987a. Parent-offspring resource allocation in Swallows during nestling rearing: an experimental study. Ardea 75, 145–168.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 223

223

JONES, G. 1987b. Parental foraging ecology and feeding behaviour during nestling rearing in the Swallow. Ardea 75, 169–174. JONES, G. 1987c. Time and energy constraints during incubation in free-living Swallows (Hirundo rustica): an experimental study using precision electronic balances. Journal of Animal Ecology 56, 229–245. JONES, G. 1988. Concurrent demands of parent and offspring Swallows Hirundo rustica in a variable feeding environment. Ornis Scandinavica 19, 145–152. JONES, G. 1989. Optimizing time off the nest during incubation in female Swallows Hirundo rustica [L.]. Functional Ecology 3, 303–309. KABUS, A. 2002. Hybriden zwischen Rauchschwalbe Hirundo rustica und Mehlschwalbe Delichon urbica. Limicola 16, 276–285. KANG, K-W. 1971. Foreign recoveries of House Swallows banded in eastern Asian countries. Ostrich 42, 179–189. KANNAN, K., CORSOLINI, S., IMAGAWA, T., FOCARDI, S. & GIESY, J. P. 2002. Polychlorinatednaphthalenes, -biphenyls, -dibenzo-p-dioxins, dibenzofurans and p,p’-DDE in bluefin tuna, swordfish, cormorants and Barn Swallows from Italy. Ambio 31, 207–211. KARTANAS, E. 2001. [Numbers of breeding populations of Swallow Hirundo rustica L. and House-Martin Delichon urbica (L.) in an agricultural area near Torun´.] Acta Universitas Nicolai Copernici 107, 3–33 [in Polish]. KEIGHLEY, M. & HALL, A. 1995. Grey heron capturing hirundine in flight. British Birds 88, 423. KEITH, A. R., WILEY, J. W., LATTA, S. C. & OTTENWALDER, J. A. 2003. The Birds of Hispaniola. BOU, Tring. KEITH, S., URBAN, E. K. & FRY, C. H. 1992. The Birds of Africa. Volume IV. Academic Press, London. KENDEIGH, S. C. 1952. Parental care and its evolution in birds. Illinois Biological Monographs 22, 1–356. KILGORE, D. L. & KNUDSEN, K. L. 1977. Analysis of materials in Cliff and Barn Swallow nests: relationship between mud selection and nest architecture. Wilson Bulletin 89, 562–571. KILNER, R. & DAVIES, N. B. 1998. Nestling mouth colour: ecological correlates of a begging signal. Animal Behaviour 56, 705–712. KING, B. 1988. Migrating swallows feeding juveniles in flight. British Birds 88, 182. KING, B. & PENHALLURICK, R. D. 1977. Swallows wintering in Cornwall. British Birds 70, 341. KING, K. A., CUSTER, T. W. & WEAVER, D. A. 1994. Reproductive success of Barn Swallows nesting near a selenium-contaminated lake in east Texas, USA. Environmental Pollution 84, 53–58. KINGERY, H. E. 1998. Colorado Breeding Bird Atlas. Bird Atlas Partnerships, Denver. KISTCHINSKIY, A. A. 1980. [Birds of Koryak Upland.] Moscow, Nauka Press [in Russian]. KLEVEN, O., JACOBSEN, F., IZADNEGAHDAR, R., ROBERTSON, R. J. & LIFJELD, J. T. In press a. No evidence of paternal genetic contribution to nestling cell-mediated immunity in the North American Barn Swallow. Animal Behaviour. KLEVEN, O., JACOBSEN, F., IZADNEGAHDAR, R., ROBERTSON, R. J. & LIFJELD, J. T. In press b. Male tail streamer length predicts fertilization success in the North American Barn Swallow (Hirundo rustica erythrogaster). Behavioral Ecology and Sociobiology. KLOMP, H. 1970. The determination of clutch size in birds. A review. Ardea 58, 1–124. KNOX, A. 1992. Extended foraging period of nesting Swallows. British Birds 83, 166.

14639.qxd

24/1/06

224

3:54 pm

Page 224

Bibliography

KOHLI, L., GRAF, R., KESTENHOLZ, M. & SCHIFFERLI, L. 2004. Vôgel in Kulturland. Schweizerische Vogelwarte Sempach. KOLOYARTSEV, M. V. 1960. The diet of House Martins and Swallows in the Leningrad Region. Synopses of Reports of the 4th Baltic Region Ornithological Conference, Riga 50–51. KOMAROV, Y. E. 2000. [Nesting biology of the Barn Swallow in Northern Ossetia.] Caucasian Ornithological Bulletin 12, 133–137 [in Russian]. KONDELKA, D. 1985. Gelegegrösse und Brutverluste der Rauchschwalbe (Hirundo rustica) im Nordmährischen Kreis (CˇSSR). Folia Zoologica 34, 149–158. KONSTANTINOV, V., NOWICKI, W. & PICHURIN, A. 1996. Recent changes in the avifaunas of cities in European Russia and eastern Poland. Results of a questionnaire. Acta Ornithologica 31, 59–66. KOPACHENA, J. G., BUCKLEY, A. J. & POTTS, G. A. 2000. Effects of the red imported fire ant (Solenopsis invicta) on reproductive success of Barn Swallows (Hirundo rustica) in north-east Texas. Southwestern Naturalist 45, 477–482. KOPIJ, G. 2000. Diet of swifts (Apodidae) and swallows (Hirundinidae) during the breeding season in South African grassland. Acta Ornithologica 35, 203–206. KOSE, M. 1994. [On the monitoring of swallows in Estonia.] Hirundo 2, 52–58 [in Estonian]. KOSE, M. 2001. Suitsupääsuke- Aasta Lind 2000. Hirundo 14, 3–10. KOSE, M. & MØLLER, A. P. 1999. Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the Barn Swallow (Hirundo rustica). Behavioral Ecology and Sociobiology 45, 430–436. KOSE, M., MÄND, R. & MØLLER, A. P. 1999. Sexual selection for white tail spots in the Barn Swallow in relation to habitat choice by feather lice. Animal Behaviour 58, 1201–1205. KOSTIN, Y. V. 1983. [Birds of the Crimea]. Moscow, Nauka Press [in Russian]. KOZENA, I. 1979. A study of the qualitative composition of the diet of young Swallows (Hirundo rustica) in an agricultural farm. Folia Zoologica 28, 337–346. KOZENA, I. 1980. Dominance of items and diversity of the diet of young Swallows (Hirundo rustica). Folia Zoologica 29, 143–156. KOZENA, I. 1983. Comparison of the diets of young Swallows (Hirundo rustica) and House Martins (Delichon urbica). Folia Zoologica 32, 41–50. KOZMA, J. M. & MATHEWS, N. E. 1995. Interspecific cooperative nesting between Barn Swallows and Say’s Phoebes in south-central New Mexico. Auk 112, 515–517. KREN, J. 2000. Birds of the Czech Republic. Christopher Helm, London. KUDRYAVTSEVA, M. Y. 1997. [Formation of additional juvenile feathering in the Barn Swallow Hirundo rustica]. Russian Journal of Ornithology 10, 17–19 [in Russian]. KUZNIAK, S. 1967. Observations on the breeding biology of Swallow, Hirundo rustica L. Acta Ornithologica 30, 177–211. LACK, D. 1947. The significance of clutch size. Ibis 89, 302–352. LACK, P. 1986. The Atlas of Wintering Birds in Britain and Ireland. T & A D Poyser, London. LANDMANN, A. & LANDMANN, C. 1978. Zur Siedlungsbiologie der Rauchschwalbe Hirundo rustica und Mehlschwalbe Delichon urbica in der Unteren Schranne, Nordtirol. Anzeiger der Ornithologischen Gesellschafts Bayern 17, 247–246. LANGUY, M. & VANSTEENWEGEN, C. 1989. Influence of parental age on the growth of nestling Swallows Hirundo rustica. Ardea 77, 227–232. LEHIKOINEN, E., SPARKS, T. H. & ZALAKEVICIUS, M. 2004. Arrival and departure dates. Advances in Ecological Research 35, 1–31.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 225

225

LEWIS, T. & TAYLOR, L. R. 1965. Diurnal periodicity of flight by insects. Transactions of the Royal Entomological Society of London 116, 393–476. LIECHTI, F. & BRUDERER, L. 2002. Wingbeat frequency of Barn Swallows and House Martins: a comparison between free flight and wind tunnel experiments. Journal of Experimental Biology 205, 2461–2467. LIGUE POUR LA PROTECTION DES OISEAUX 2004. Empoisonnement de 100 hirondelles aux insecticides. http://www.lpo.fr/comm/2004/comm2004–07–01a.shtml LOESCHE, P., STODDARD, P. K., HIGGINS, B. J. & BEECHER, M. D. 1991. Signature versus perceptual adaptations for individual vocal recognition in swallows. Behaviour 118, 15–25. LOHOEFENER, R. R 1977. Comparative Nesting Ecology of Solitary and Colonial Nesting Barn Swallows in West-Central Kansas. M.S. thesis, Fort Hays State University. LOHOEFENER, R. R 1980. Comparative Breeding Biology and Ecology of Colonial and Solitary Nesting Barn Swallows (Hirundo rustica) in East-Central Mississippi. Ph.D. thesis, Mississippi State University. LÖHRL, H. & GUTSCHER, H. 1973. Zur Brutbiologie der Rauchschwalbe (Hirundo rustica) in einem südwestdeutschen Dorf. Journal für Ornithologie 114, 399–416. LOREK, G. 1992. [Breeding biology of Chimney Swallow Hirundo rustica in southern Wielkopolska.] Lubuski Przeglad Przyrodniczy 3, 71–83 [in Polish]. LOSKE, K. H. 1982. Zum Umsiedlungsverhalten von Altvögeln bei der Rauchschwalbe (Hirundo rustica). Journal für Ornithologie 123, 106. LOSKE, K. H. 1984. Beobachtungen an mittelwestfälischen Schlafplätzen der Rauchschwalbe (Hirundo rustica). Vogelwelt 105, 51–60. LOSKE, K. H. 1986. The origins of European Swallows wintering in Namibia and Botswana. Ringing & Migration 7, 119–121. LOSKE, K. H. 1989. Zur Brutbiologie der Rauchschwalbe (Hirundo rustica) in Mittelwestfalen. Vogelwelt 109, 59–82. LOSKE, K. H. 1990a. Zum Wegzug der Rauchschwalbe Hirundo rustica in Mittelwestfalen. Vogelwelt 111, 122–141. LOSKE, K. H. 1990b. Zur Biometrie und Gewichtsentwicklumg der Rauchschwalbe (Hirundo rustica) in Mittelwestfalen. Vogelwarte 35, 186–201. LOSKE, K. H. 1992. Nestlingsnahrung der Rauchschwalbe (Hirundo rustica) in Mittelwestfalen. Vogelwarte 36, 173–187. LOSKE K. H. 1994. Untersuchungen zu Überlebensstrategien der Rauchschwalbe (Hirundo rustica) im Brutgebiet. Ph.D. thesis, Rheinischen Friedrich-Wilhelms-Universität Bonn. LOSKE, K. H 1996. Ein wichtiger Schlafplatz europäischer Rauchschwalben Hirundo rustica und seine Bedrohung. Limicola 10, 42–48. LOSKE, K. H 1999. Massenfang von Rauchschwalben Hirundo rustica in Nigeria gestoppt: Erfolg der Spendenaktion. Limicola 13, 278–280. LOSKE, K. H. & LEDERER, W. 1987. Bestandsentwicklung und Fluktuationsrate von Weitstreckenziehern in Westfalen: Uferschwalbe (Riparia riparia), Rauchschwalbe (Hirundo rustica), Baumpieper (Anthus trivialis) und Grauschnäpper (Muscicapa striata). Charadrius 23, 101–127. LOTEM, A. 1998a. Higher levels of begging behavior by small nestlings: a case of a negatively correlated handicap. Israel Journal of Zoology 44, 29–45. LOTEM, A. 1998b. Differences in begging behaviour between Barn Swallow, Hirundo rustica, nestlings. Animal Behaviour 55, 809–818.

14639.qxd

24/1/06

226

3:54 pm

Page 226

Bibliography

LYAKHOV, A. G. & GUSEV, Y. K. 2001. [Prolonged delay of autumn departure in the Barn Swallow Hirundo rustica.] Russian Journal of Ornithology, 140, 321–322 [in Russian]. LYNCH, B. M. 1982. Mass and population structure of emigrating Swallows (Hirundo rustica) in roosts in Tayside (1972–1982). Tay Ringing Group Report 28–44. LYULEEVA, D. S. 1973 Features of swallow biology during migration. In Bykhovskii, B. E., Bird Migrations: Ecological and Physiological Factors, pp. 219–272. J. Wiley, Chichester. MAL’CHEVSKIY, A. S. & PUKINSKIY, Yu. B. 1983. [Birds of the Leningrad Region and Adjoining Areas. History, Biology, Conservation.] Volume 2. Leningrad University Press [in Russian]. MALLORY, M. L., RENDELL, W. B. & ROBERTSON, R. J. 2000. Responses of birds to broken eggs in their nests. Condor 102, 673–675. MARKS, L. P. 1982. [Breeding biology of swallows (Riparia riparia, Hirundo rustica) in the south of Western Siberia.] Candidate of Biological Sciences dissertation summary, Sverdlosk [in Russian]. MARTIN, R. F. 1980. Analysis of hybridization between the hirundinid genera Hirundo and Petrochelidon in Texas. Auk 97, 148–159. MARTINEZ, M .M. 1983. Nidificacion de Hirundo rustica erythrogaster (Boddaert) en la Argentina (Aves, Hirundinidae). Neotropica 29, 83–86. MARTINS, T. L. F. 1997. Fledging in the Common Swift, Apus apus: weight-watching with a difference. Animal Behaviour 54, 99–108. MASON, C. F. 1995. Long-term trends in the arrival dates of spring migrants. Bird Study 42, 182–189. MASON, E. A. 1953. Barn Swallow life history data based on banding records. Bird-Banding 24, 91–100. MASSI, A., FOSSI, C., LARI, L., LEONZIO, C., CASINI, S. & FERRO, G. 1991. Effetto dell’uso di insetticidi organofosforici sul livello delle esterase ematiche in esemplari di rondine, Hirundo rustica. Rivista Italiana di Ornitologia Milano 61, 101–106. MATYJASIAK, P. & JABLONSKI, P. G. 2001. Hypothetical mechanisms of the initial evolution of sexually dimorphic tail streamers in Hirundinidae. Evolution 55, 446–448. MATYJASIAK, P., JABLONSKI, P. G., OLEJNICZAK, I., BONIECKI, P. I. & LEE, S. D. 1999. Foraging cost of a long tail ornament: an experiment with Sand Martin females. Ethology 105, 521–530. MATYJASIAK, P., JABLONSKI, P. G., OLEJNICZAK, I. & BONIECKI, P. I. 2000a. Imitating the initial evolutionary stage of a tail ornament. Evolution 54, 704–711. MATYJASIAK, P., JABLONSKI, P. G., OLEJNICZAK, I., BONIECKI, P. I. & LEE, S. D. 2000b. Examining the cost of experimentally imitated ornaments. Ethology 106, 665–668. MATYJASIAK, P., MATYJASIAK, J., DE LOPE, F. & MØLLER, A. P. 2004. Vane emargination of outer tail feathers improves flight manoeuvrability in streamerless hirundines, Hirundinidae. Proceedings of the Royal Society of London B 271, 1831–1838. MAUTE, K. L. 2003. Note on longevity of North American birds. North American Bird Bander 28, 13–14. MCATEE, W. L. 1947. Torpidity in birds. American Midland Naturalist 38, 191–206. MCCARTY, J. P. & SECORD, A. L. 1999a. Reproductive ecology of Tree Swallows (Tachycineta bicolor) with high levels of polychlorinated biphenyl contamination. Environmental Toxicology and Chemistry 18, 1433–1439. MCCARTY, J. P. & SECORD, A. L. 1999b. Nest-building behavior in PCB-contaminated Tree Swallows. Auk 116, 55–63.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 227

227

MCCARTY, J. P. & SECORD, A. L. 2000. Possible effects of PCB contamination on female plumage color and reproductive success in Hudson River Tree Swallows. Auk 117, 987–995. MCCLURE, H. E. 1974. Migration and Survival of the Birds of Asia. US Medical Component, SEATO Medical Project, Bangkok. MCGINN, D. B. 1979. Status and breeding biology of Swallows in Banffshire. Scottish Birds 10, 221–229. MCGINN, D. B. & CLARK, H. 1978. Some measurements of Swallow breeding biology in lowland Scotland. Bird Study 25, 109–118. MCGRAW, K. J., WAKAMATSU, K., ITO, S., NOLAN, P. M., JOUVENTIN, P., DOBSON, F. S., AUSTIC, R. E., SAFRAN, R. J., SIEFFERMAN, L. M., HILL, G. E. & PARKER, R. S 2004a. You can’t judge a pigment by its color: carotenoid and melanin content of yellow and brown feathers in swallows, bluebirds, penguins, and domestic chickens. Condor 106, 390–395. MCGRAW, K. J., SAFRAN, R. J., EVANS, M. R. & WAKAMATSU, K. 2004b. European Barn Swallows use melanin pigments to color their feathers brown. Behavioral Ecology 15, 889–891. MCKECHNIE, A. E. & LOVEGROVE, B. G. 2002. Avian facultative hypothermic responses: a review. Condor 104, 705–724. MCKITRICK, M. C. 1993. Trends in the evolution of hindlimb musculature in aerial-foraging birds. Auk 110, 189–206. MCNAMARA, J. M. & HOUSTON, A. I. 1990. The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheoretica 38, 37–61. MCWILLIAMS, G. M. & BRAUNING, D. W. 2000. The Birds of Pennsylvania. Cornell University Press, Ithaca. MEAD, C. J. 1970. The winter quarters of British Swallows. Bird Study 17, 227–240. MEAD, C. J. 2002. Barn Swallow. In Wernham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. & Baillie, S. R. (eds), The Migration Atlas: Movements of the Birds of Britain and Ireland, pp. 462–464. T & A D Poyser, London. MEAD, C. J. & CLARK, J. A. 1987. Report on bird ringing for 1986. Ringing and Migration 8, 135–200. MEAD, C. J. & HARRISON, J. D. 1979. Sand Martin movements within Britain and Ireland. Bird Study 12, 151–169. MEAD, C. J. & PEPLER, G. R. M. 1975. Birds and other animals at Sand Martin colonies. British Birds 68, 89–99. MEDVIN, M. M. & BEECHER, M. D. 1986. Parent-offspring recognition in the Barn Swallow (Hirundo rustica). Animal Behaviour 34, 1627–1639. MEDVIN, M. M., BEECHER, M. D. & ANDELMAN, S. J. 1987. Extra adults at the nest in Barn Swallows. Condor 89, 179–182. MEDVIN, M. B., STODDARD, P. K. & BEECHER, M. D. 1992. Signals for parent-offspring recognition: strong sib-sib call similarity in Cliff Swallows but not Barn Swallows. Ethology 80, 17–28. MEDVIN, M. B., STODDARD, P. K. & BEECHER, M. D. 1993. Signals for parent-offspring recognition: a comparative analysis of the begging calls of Cliff Swallows and Barn Swallows. Animal Behaviour 45, 841–850. MEDWAY, Lord 1973. A ringing study of migratory Barn Swallows in west Malaysia. Ibis 115, 60–86. MEIER, W. 2001. Rauch- und Mehlschwalbenzählung in Anraff im Jahr 2000 mit einer vergleichenden Betrachtung der Bestandentwicklung über einen Zeitraum von vier Jahrzehnten. Vogelkunde Hefte Edertal 27, 8–26.

14639.qxd

24/1/06

228

3:54 pm

Page 228

Bibliography

MERINO, S., MØLLER, A. P. & DE LOPE, F. 2000. Seasonal changes in cell-mediated immunocompetence and mass gain in nestling Barn Swallows: a parasite-mediated effect? Oikos 90, 327–332. MERRILL, J. P. 1976. Oyster shells attract Barn Swallows. East Bird-Banding News 39, 20–21. MERZLIKIN, I. R. 2001. [Capture of fishes by swallows.] Berkut 10, 120 [in Russian]. MESERVEY, W.R. & KRAUS, G.F. 1976. Absence of ‘individual distance’ in three swallow species. Auk 93, 177–179. MICHELONI, P. 2003. Ebbaken. http://www.swallowschool.it/ingl/obiet_africa/ebbaken2.html MILLARD, J. B., WHICKER, F. W. & MARKHAM, O. D. 1990. Radionuclide uptake and growth of Barn Swallows nesting by radioactive leaching ponds. Health Physics 58, 429–439. MIZUTA, K. 1963. Local distribution of two swallows of genus Hirundo, and breeding success of H. rustica. Researches in Population Ecology 5, 130–138. MØLLER, A. P. 1982. Clutch size in relation to nest size in the Swallow Hirundo rustica. Ibis 124, 339–343. MØLLER, A. P. 1983. Breeding habitat selection in the Swallow Hirundo rustica. Bird Study 30, 134–142. MØLLER, A. P. 1984a. Parental defence of offspring in the Barn Swallow. Bird Behaviour 5, 110–117. MØLLER, A. P. 1984b. Geographical trends in breeding parameters of Swallows, Hirundo rustica, and House Martins, Delichon urbica. Ornis Scandinavica 15, 43–54. MØLLER, A. P. 1985. Mixed reproductive strategy and mate guarding in a semi-colonial passerine, the Swallow Hirundo rustica. Behavioral Ecology and Sociobiology 17, 401–408. MØLLER, A. P. 1987a. Extent and duration of mate guarding in Swallows Hirundo rustica. Ornis Scandinavica 18, 95–100. MØLLER, A. P. 1987b. Nest lining in relation to the nesting cycle in the Swallow Hirundo rustica. Ornis Scandinavica 18, 148–149. MØLLER, A. P. 1987c. Intraspecific nest parasitism and anti-parasite behaviour in Swallows, Hirundo rustica. Animal Behaviour 35, 247–254. MØLLER, A. P. 1987d. Advantages and disadvantages of coloniality in the Swallow, Hirundo rustica. Animal Behaviour 35, 819–832. MØLLER, A. P. 1987e. Mate guarding in the Swallow Hirundo rustica. An experimental study. Behavioral Ecology and Sociobiology 21, 119–123. MØLLER, A. P. 1987f. Behavioural aspects of sperm competition in Swallows (Hirundo rustica). Behaviour, 100, 92–104. MØLLER, A. P. 1988a. Female choice selects for male sexual tail ornaments in the monogamous Swallow. Nature 332, 640–642. MØLLER, A. P. 1988b. Infanticidal and anti-infanticidal strategies in the Swallow Hirundo rustica. Behavioral Ecology and Sociobiology 22, 365–371. MØLLER, A. P. 1988c. Paternity and paternal care in the Swallow, Hirundo rustica. Animal Behaviour 36, 996–1005. MØLLER, A. P. 1989a. Population dynamics of a declining Swallow Hirundo rustica population. Journal of Animal Ecology 58, 1051–1063. MØLLER, A. P. 1989b. Intraspecific nest parasitism in the Swallow Hirundo rustica: the importance of neighbors. Behavioral Ecology and Sociobiology 25, 33–38. MØLLER, A. P. 1989c. Viability costs of male tail ornaments in a swallow. Nature 339, 132–135.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 229

229

MØLLER, A. P. 1990a Effects of parasitism by a haematophagous mite on reproduction in the Barn Swallow. Ecology 71, 2345–2357. MØLLER, A. P. 1990b Effects of a haematophagous mite on the Barn Swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution 44, 771–784. MØLLER, A. P. 1990c. Deceptive use of alarm calls by male Swallows, Hirundo rustica: a new paternity guard. Behavioral Ecology 1, 1–6. MØLLER, A. P. 1990d. Male tail length and female mate choice in the monogamous Swallow, Hirundo rustica. Animal Behaviour 39, 458–465. MØLLER, A. P. 1990e. Changes in the size of avian breeding territories in relation to the nesting cycle. Animal Behaviour 40, 1070–1079. MØLLER, A. P. 1991a. Ectoparasite loads affect optimal clutch size in Swallows. Functional Ecology 5, 351–359. MØLLER, A. P. 1991b. Parasites, sexual ornaments and mate choice in the Barn Swallow. In Loye, J. E. & Zuk, M. (eds), Bird-Parasite Interactions, pp. 328–343. Oxford University Press, New York. MØLLER, A. P. 1991c. The effect of feather nest lining on reproduction in the Swallow Hirundo rustica. Ornis Scandinavica 22, 396–400. MØLLER, A. P. 1991d. Sexual selection in the monogamous Barn Swallow (Hirundo rustica). I. Determinants of tail ornament size. Evolution 45, 1823–1836. MØLLER, A. P. 1991e. Density-dependent extra-pair copulations in the Swallow Hirundo rustica. Ethology 87, 316–329. MØLLER, A. P. 1991f. Parasite load reduces song output in a passerine bird. Animal Behaviour 41, 723–730. MØLLER, A. P. 1991g. The preening activity of Swallows, Hirundo rustica, in relation to experimentally manipulated loads of haematophagous mites. Animal Behaviour 42, 251–260. MØLLER, A. P. 1991h. Defence of offspring by male Swallows, Hirundo rustica, in relation to participation in extra-pair copulations by their mates. Animal Behaviour 42, 261–267. MØLLER, A. P. 1991i. Double broodedness and mixed reproductive strategies by female Swallows. Animal Behaviour 42, 671–679. MØLLER, A. P. 1991j. Sexual ornament size and the cost of fluctuating asymmetry. Proceedings of the Royal Society of London B 243, 59–62. MØLLER, A. P. 1991k. Viability is positively related to degree of ornamentation in male Swallows. Proceedings of the Royal Society of London B 243, 145–148. MØLLER, A. P. 1991l. Preferred males get mates of higher phenotypic quality. Proceedings of the Royal Society of London B 245, 179–182. MØLLER, A. P. 1991m. Why mated songbirds sing so much: mate guarding and male announcement of mate fertility status. American Naturalist 138, 994–1014. MØLLER, A. P. 1992a. Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters. Journal of Evolutionary Biology 5, 691–699. MØLLER, A. P. 1992b. Sexual selection in the monogamous Barn Swallow Hirundo rustica 2. Mechanisms of sexual selection. Journal of Evolutionary Biology 5, 603–624. MØLLER, A. P. 1992c. Frequency of female copulations with multiple males and sexual selection. American Naturalist 139, 1089–1101. MØLLER, A. P. 1992d. Female Swallow preference for symmetrical male sex ornaments. Nature 357, 238–240.

14639.qxd

24/1/06

230

3:54 pm

Page 230

Bibliography

MØLLER, A. P. 1993a. Ectoparasites increase the cost of reproduction in their hosts. Journal of Animal Ecology 62, 309–322. MØLLER, A. P. 1993b. Morphology and sexual selection in the Barn Swallow Hirundo rustica in Chernobyl, Ukraine. Proceedings of the Royal Society of London B 252, 51–57. MØLLER, A. P. 1993c. Sexual selection in the Barn Swallow Hirundo rustica. III. Female tail ornaments. Evolution 47, 417–431. MØLLER, A. P. 1993d. Female preference for apparently symmetrical male sexual ornaments in the Barn Swallow Hirundo rustica. Behavioral Ecology and Sociobiology 32, 371–376. MØLLER, A. P. 1994a. Sexual Selection and the Barn Swallow. Oxford University Press, Oxford. MØLLER, A. P. 1994b. Parasite infestation and parental care in the Barn Swallow Hirundo rustica: a test of the resource-provisioning model of parasite-mediated sexual selection. Ethology 97, 215–225. MØLLER, A. P. 1994c. Sexual selection in the Barn Swallow (Hirundo rustica). IV. Patterns of fluctuating asymmetry and selection against asymmetry. Evolution 48, 658–670. MØLLER, A. P. 1994d. Symmetrical male sexual ornaments, paternal care, and offspring quality. Behavioral Ecology 5, 188–194. MØLLER, A. P. 1994e. Repeatability of female choice in a monogamous swallow. Animal Behaviour 47, 643–648. MØLLER, A. P. 1994f. Phenotype-dependent arrival time and its consequences in a migratory bird. Behavioral Ecology and Sociobiology 35, 115–122. MØLLER, A. P. 1994g. Male ornament size as a reliable cue to enhanced offspring viability in the Barn Swallow. Proceedings of the National Academy of Sciences USA 91, 6929–6932. MØLLER, A. P. 1995. Sexual selection in the Barn Swallow Hirundo rustica. V. Geographic variation in ornament size. Journal of Evolutionary Biology 8, 3–19. MØLLER, A. P. 1996a. Development of fluctuating asymmetry in tail feathers of the Barn Swallow Hirundo rustica. Journal of Evolutionary Biology 9, 677–694. MØLLER, A. P. 1996b. The cost of secondary sexual characters and the evolution of cost-reducing traits. Ibis 138, 112–119. MØLLER, A. P. 1997. Parasitism and the evolution of host life history. In Clayton, D. H. & Moore, J. (eds), Host-Parasite Evolution. General Principles and Avian Models, pp. 105–127. Oxford University Press, Oxford. MØLLER, A. P. 2000. Male parental care, female reproductive success, and extrapair paternity. Behavioral Ecology 11, 161–168. MØLLER, A. P. 2001a. Heritability of arrival date in a migratory bird. Proceedings of the Royal Society of London B 268, 203–206. MØLLER, A. P. 2001b. The effect of dairy farming on Barn Swallow Hirundo rustica abundance, distribution and reproduction. Journal of Applied Ecology 38, 378–389. MØLLER, A. P. 2001c. Sexual selection in the Barn Swallow. In Dugatkin, L. A. (ed.), Model Systems in Behavioral Ecology, pp. 359–377. Princeton University Press, Princeton. MØLLER, A. P. 2002a. Parent-offspring resemblance in degree of sociality in a passerine bird. Behavioral Ecology and Sociobiology 51, 276–281. MØLLER, A. P. 2002b. Temporal change in mite abundance and its effect on Barn Swallow reproduction and sexual selection. Journal of Evolutionary Biology 15, 495–504. MØLLER, A. P. 2002c. North Atlantic Oscillation (NAO) effects of climate on the relative importance of first and second clutches in a migratory passerine bird. Journal of Animal Ecology 71, 201–210.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 231

231

MØLLER, A. P. 2004a. Rapid temporal change in frequency of infanticide in a passerine bird associated with change in population density and body condition. Behavioral Ecology 15, 462–468. MØLLER, A. P. 2004b. Protandry, sexual selection and climate change. Global Change Biology 10, 2028–2035. MØLLER, A. P. & BARBOSA, A. 2001. Flight, fitness and sexual selection. Behavorial Ecology 12, 511–512. MØLLER, A. P. & DE LOPE, F. 1994. Differential costs of a secondary sexual character: an experimental test of the handicap principle. Evolution 48, 1676–1683. MØLLER, A. P. & DE LOPE, F. 1995. Differential allocation and sexual ornamentation. Evolution 49, 1290–1292. MØLLER, A. P. & DE LOPE, F. 1999. Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. Journal of Animal Ecology 68, 163–171. MØLLER, A. P. & HOBSON, K. A. 2004. Heterogeneity in stable isotope profiles predicts coexistence of populations of Barn Swallows Hirundo rustica differing in morphology and reproductive performance. Proceedings of the Royal Society of London B 271, 1355–1362. MØLLER, A. P. & MOUSSEAU, T. A. 2001. Albinism and phenotype of Barn Swallows Hirundo rustica from Chernobyl. Evolution 55, 2097–2104. MØLLER, A. P. & NIELSEN, J. T. 1997. Differential predation cost of a secondary sexual character: Sparrowhawk predation on Barn Swallows. Animal Behaviour 54, 1545–1551. MØLLER, A. P. & SAINO, N. 2004. Immune response and survival. Oikos 104, 299–304. MØLLER, A. P. & SWADDLE, J. P. 1997. Asymmetry, Developmental Stability, and Evolution. Oxford University Press, Oxford. MØLLER, A. P. & SZÉP, T. 2002. Survival rate of adult Barn Swallows Hirundo rustica in relation to sexual selection and reproduction. Ecology 83, 2220–2228. MØLLER, A. P. & SZÉP, T. 2005a. Age-dependent reproduction, environmental conditions and climate change. Oecologia in press. MØLLER, A. P. & SZÉP, T. 2005b. Rapid evolutionary change in a secondary sexual character linked to climatic change. Journal of Evolutionary Biology 18, 481–495. MØLLER, A. P. & TEGELSTRÖM, H. 1997. Extra-pair paternity and tail ornamentation in the Barn Swallow Hirundo rustica. Behavioral Ecology and Sociobiology 41, 353–360. MØLLER, A. P. & VANSTEENWEGEN, C. 1997. Swallow. In Hagemeijer, W. J. M. & Blair, M. J. (eds), The EBCC Atlas of European Breeding Birds, pp. 478–479. T & A D Poyser, London. MØLLER, A. P., DE LOPE, F. & CABALLERO, J. M. L. 1995a. Foraging costs of a tail ornament: experimental evidence from two populations of Barn Swallows Hirundo rustica with different degrees of sexual size dimorphism. Behavioral Ecology and Sociobiology 37, 289–295. MØLLER, A. P., MAGNHAGEN, C., ULFSTRAND, A & ULFSTRAND, S. 1995b. Phenotypic quality and molt in the Barn Swallow, Hirundo rustica. Behavioral Ecology 6, 242–249. MØLLER, A. P., DE LOPE, F. & SAINO, N. 1995c. Sexual selection in the Barn Swallow Hirundo rustica. VI. Aerodynamic adaptations. Journal of Evolutionary Biology 8, 671–687. MØLLER, A. P., SAINO, N., TARAMINO, G., GALEOTTI, P. & FERRARIO S. 1998a. Paternity and multiple signaling: effects of a secondary sexual character and song on paternity in the Barn Swallow. American Naturalist 151, 236–242. MØLLER, A. P., BARBOSA, A., CUERVO, J. J., DE LOPE, F., MERINO, S. & SAINO, N. 1998b. Sexual selection and tail streamers in the Barn Swallow. Proceedings of the Royal Society of London B 265, 409–414.

14639.qxd

24/1/06

232

3:54 pm

Page 232

Bibliography

MØLLER, A. P., MERINO, S., BROWN, C. R. & ROBERTSON, R. J. 2001 Immune defense and host sociality: a comparative study of swallows and martins. American Naturalist 158, 136–145. MØLLER, A. P., BROHEDE, J., CUERVO, J. J., DE LOPE, F. & PRIMMER, C. 2003. Extra-pair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird. Behavioral Ecology 14, 707–712. MØLLER, A. P., MARTINELLI, R. & SAINO, N. 2004a. Genetic variation in infestation with a directly transmitted ectoparasite. Journal of Evolutionary Biology 17, 41–47. MØLLER, A. P., DE LOPE, F. & SAINO, N. 2004b. Parasitism, immunity and arrival date in a migratory bird, the Barn Swallow. Ecology 85, 206–219. MORALES FERNAZ, J. 2001. Illustrated Guide to Aging Nestling Barn Swallows (Hirundo rustica): Nestling Growth and Development of Body and Plumage Body Mass, Feather Length. Manuscript, Swiss Ornithological Institute. MORAND, M. 2000. Food Supply for Barn Swallows Hirundo rustica in the Agricultural Land of the Wauwilermoos (Lucerne). Diploma thesis, University of Geneva and Swiss Ornithological Institute, Sempach. MOREAU, R. E. 1961. Problems of Mediterranean-Saharan migration. Ibis 103a, 373–427. MOREAU, R. E. 1972. The Palaearctic-African Bird Migration System. Academic Press, London. MOREAU, R. E. & MOREAU, W. M. 1939. Observations on Swallows and House Martins at the nest. British Birds 33, 146–151. MORENO, E. & MØLLER, A. P. 1996. Morphological aspects of avian tail movements: a functional approach in hirundines. Auk 113, 647–654. MORENO, J. 1989. Strategies of mass change in breeding birds. Biological Journal of the Linnean Society 37, 297–310. MUNTEANU, D. 1998. The Status of Birds in Romania. Romanian Ornithological Society, Bucharest. MURANO, N., HIGUCHI, T. & OKABE, T. 2000. [Breeding status of the Barn Swallow (Hirundo rustica) surveyed in Hokkaido, Japan.] Journal of Rakuno Gakuen University Natural Science, 25, 95–101 [in Japanese]. MURPHY, M. E. 1996. Energetics and nutrition of molt. In Carey, C. (ed.), Avian Energetics and Nutritional Ecology, pp. 158–198. Chapman & Hall, New York. MURRAY, R., HOLLING, M., DOTT, H. & VANDOME, P. 1998. The Breeding Birds of South-east Scotland: A Tetrad Atlas 1988–1994. Scottish Ornithologists’ Club, Edinburgh. MYERS, G. R. & WALLER, D. W. 1977. Helpers at the nest in Barn Swallows. Auk 94, 596. NEWTON, I. 1989. Lifetime Reproduction in Birds. Academic Press, London. NICHOLSON, C. P. 1997. Atlas of the Breeding Birds of Tennessee. University of Tennessee Press, Knoxville. NICOLAU-GUILLAMET, P. 1998. L’Hybridation Hirondelle Rustique Hirundo rustica x Hirondelle de Fenêtre Delichon urbica: mythe ou réalité? Alauda 66, 283–297. NIKOLAEV, V.I. 1998. [Birds of the marsh landscapes of ‘Zavidovo’ National Park and Upper Volga River area.] Tver’, State Complex ‘Zavidovo’ 140–141 [in Russian]. NILSSON, J-A. 1993. Bisexual incubation facilitates hatching asynchrony. American Naturalist 142, 712–717. NINNI, P., DE LOPE, F., SAINO, N., HAUSSY, C. & MØLLER, A. P. 2004. Antioxidants and conditiondependence of arrival date in a migratory bird. Oikos 105, 55–64. NORBERG, R. Å. 1981. Temporary weight decrease in breeding birds may result in more fledged young. American Naturalist 118, 838–850.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 233

233

NORBERG, R. Å. 1994. Swallow tail streamer is a mechanical device for self-deflection of tail leading edge, enhancing aerodynamic efficiency and flight manoeuvrability. Proceedings of the Royal Society of London B 257, 227–233. NUDDS, R. L. & SPENCER, K. A. 2004. Daily energy expenditure of male Barn Swallows correlates with tail-streamer length: handicap-mediated foraging strategies. Proceedings of the Royal Society of London B 271, S160–S163. NUTTALL, R. J. 1998. European Swallows roosting in suburban Bloemfontein. Mirafra 15, 37–38. NUTTALL, R. J. 2003. The Bloemfontein Swallow project: 2001–2003. Afring News 32, 12–15. OATLEY, T. B. 2000. Migrant European Swallows Hirundo rustica in southern Africa: a southern perspective. Ostrich 71, 205–209. OBA, G., POST, E. & STENSETH, N. C. 2001. Sub-Saharan desertification and productivity are linked to hemispheric climate variability. Global Change Biology 7, 241–246. O’CONNOR, R. J. 1984. The Growth and Development of Birds. J. Wiley, Chichester. OLIVER, P. J. 1997. The breeding birds of Inner London, 1966–94. British Birds 90, 211–225. OLIVER, P. J. 2002. Barn Swallows and House Martins taking grit. British Birds 95, 23–26. OPDAM, P. 1979. Feeding ecology of a sparrowhawk population Accipiter nisus. Ardea 66 , 137–155. ORMEROD, S. J. 1989. The influence of weather on the body mass of migrating Swallows Hirundo rustica in South Wales. Ringing and Migration 10, 65–74. ORMEROD, S. J. 1991. Pre-migratory and migratory movements of Swallows Hirundo rustica in Britain and Ireland. Bird Study 38, 170–178. OWEN, D. F. 1955. Additional records of protocalliphora (Diptera) in birds’ nests. British Birds 48, 225–229. OWEN, J.H. 1918. A note on the nesting of the swallow. British Birds 11, 226. PALMER-BELL, B. Jr. 1996. The Kentucky Bird Breeding Atlas. University Press of Kentucky, Lexington. PANKHURST, T. 2005 Cuckoo parasitising Swallow. British Birds 98, 320. PAP, P. L. 2002. Breeding time and sex-specific health status in the Barn Swallow Hirundo rustica. Canadian Journal of Zoology 80, 2090–2099. PAP, P. L. & MÁRKUS, R. 2003. Cost of reproduction, T-lymphocyte mediated immunocompetence and health status in female and nestling Barn Swallows Hirundo rustica. Journal of Avian Biology 34, 428–434. PAP, P. L. & SZABÓ, D. Z. 1998. [Clutch and egg size variation in the Barn Swallow Hirundo rustica during the breeding season.] Collegium Biologicum, 2, 75–89 [in Polish]. PAP, P. L., TÖKÖLYI, J. & SZÉP, T. 2005. Frequency and consequences of feather holes in Barn Swallows Hirundo rustica. Ibis 147 , 169–175. PARADIS, E., BAILLIE, S. R., SUTHERLAND, W. J. & GREGORY, R. D. 1998. Patterns of natal and breeding dispersal in birds. Journal of Animal Ecology 67, 518–536. PARADIS, E., BAILLIE, S. R., SUTHERLAND, W. J. & GREGORY, R. D. 2002. Exploring density-dependent relationships in demographic parameters in populations of birds at a large spatial scale. Oikos 97, 293–307. PARK, K. J., EVANS, M. R. & BUCHANAN, K. L. 2000. Assessing the aerodynamic effects of tail elongations in the House Martin (Delichon urbica): implications for the initial selection pressures in hirundines. Behavioral Ecology and Sociobiology 48, 364–372. PARK, K. J., ROSÉN, M. & HEDENSTRÖM, A. 2001a. Flight kinematics of the Barn Swallow (Hirundo rustica) over a wide range of speeds in a wind tunnel. Journal of Experimental Biology 204, 2741–2750.

14639.qxd

24/1/06

234

3:54 pm

Page 234

Bibliography

PARK, K. J., BUCHANAN, K. L. & EVANS, M. R. 2001b. Sexy streamers? The role of natural and sexual selection in the evolution of hirundine tail streamers. Evolution 55, 445–446. PARSLOW, J. L. F. 1973. Breeding Birds of Britain and Ireland. T & A D Poyser, London. PATTERSON, R. M. 1981. Latitudinal variation in length of Barn Swallow tails in North America. North American Bird-Bander 6, 151–154. PAYNTER, R. A., Jr. 1995. Nearctic Passerine Migrants in South America. Nuttall Ornithological Club, Cambridge, Massachusetts. PECK, G. K. & JAMES, R. D. 1987. Breeding Birds of Ontario. Volume 2. Royal Ontario Museum, Ontario. PENG, R. K., FLETCHER, C. R. & SUTTON, S. 1992. The effect of microclimate on flying Dipterans. International Journal of Biometeorology 36, 69–76. PENNYCUICK, C. J., HEDENSTRÖM, A. & ROSÉN, M. 2000. Horizontal flight of a Swallow (Hirundo rustica) observed in a wind tunnel, with a new method for directly measuring mechanical power. Journal of Experimental Biology 203, 1755–1765. PÉREZ-TRIS, J., DE LA PUENTE, J., PINILLA, J. & BERMEJO, A. 2001. Body moult and autumn migration in the Barn Swallow Hirundo rustica: is there a cost of moulting late? Annales Zoologici Fennici 38, 139–148. PERRIER, C., DE LOPE, F., MØLLER, A. P. & NINNI, P. 2002. Structural coloration and sexual selection in the Barn Swallow Hirundo rustica. Behavioral Ecology 13, 728–736. PERRINS, C. M. 1970. The timing of birds’ breeding seasons. Ibis 112, 242–256. PETRACCI, P. F. & DELHEY, K. 2004. Nesting attempts of the Cliff Swallow Petrochelidon pyrrhonota in Buenos Aires Province, Argentina. Ibis 146, 522–525. PIKULA, J. & BEKLOVA, B. 1987. Bionomics of species of the family Hirundinidae. Acta Scientiarum Naturalium Brno 21, 1–39. PILASTRO, A. & MAGNANI, A. 1997. Weather conditions and fat accumulation dynamics in premigratory roosting Barn Swallows Hirundo rustica. Journal of Avian Biology 28, 338–344. PILASTRO, A. & SPINA, F. 1999. Fat accumulation in pre-migratory roosting Barn Swallows in Europe. In Adams, N. J. & Slotow, R. H. (eds), Proceedings of the 22nd International Ornithological Congress, Durban. BirdLife International, Johannesburg. PILASTRO, A., SPINA, F. & MICHELONI, P. 1998. Geographical variation in pre-migratory condition of Swallows Hirundo rustica in Italy. Ringing and Migration 19, 67–74. PIMM, S. L. 1972. Moult in the Swallow. Bird Study 19, 116. PONS, J-M. 1989. Contribution à l’étude de la démographie de quatre espèces de passereaux (Hirundo rustica, Delichon urbica, Parus major, Parus caeruleus) à l’échelle de la France. L’Oiseau et R.F.O. 59, 1–25. PRICE, J., DROEGE, S. & PRICE, A. 1995. The Summer Atlas of North American Birds. Academic Press, London. PRIMMER, C. R., MØLLER, A. P. & ELLEGREN, H. 1995. Resolving genetic relationships with microsatellite markers: a parentage testing system for the Swallow Hirundo rustica. Molecular Ecology 4, 493–498. PURCHON, R. D. 1948. Nesting activities of the Swallow. Proceedings of the Zoological Society of London 118, 146–170. PYLE, P. 1997. Identification Guide to North American Birds. Part 1: Columbidae to Ploceidae. State Creek Press, Bolinas, California.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 235

235

QVARNSTRÖM, A., PÄRT, T. & SHELDON, B.C. 2000. Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405, 344–347. RADERMACHER, W. 1970. Langjährige Beobachtungen an der Rauchschwalbe (Hirundo rustica). Charadrius 6, 7–23. RADERMACHER, W. 1989. Weitere Beobachtungen an der Rauchschwalben (Hirundo rustica). Charadrius 25, 179–188. RAVEN, M. J., NOBLE, D. G. & BAILLIE, S. R. 2003. The Breeding Bird Survey 2002. BTO Research Report No. 334. Thetford. REZANOV, A. G. 2003. [On the feeding behaviour of swifts and swallows during prolonged rainy and cold weather.] Russian Journal of Ornithology, 12, 660–663 [in Russian]. RHEINWALD, G. & SCHULZE-HAGEN, K. 1972. Vergleichende Untersuchungen zur Gewichtsentwicklung von Rauch- und Mehlschwalbe Hirundo rustica, Delichon urbica bei verschiedenen Witterungsbedingungen. Charadrius 8, 74–81. RIBAULT, J-P. 1982. Biologie de reproduction de quelques populations d’Hirondelles Hirundo rustica en Alsace de 1973 à 1980. Ciconia 6, 23–52. RIBAULT, J-P. 1983. Variation annuelles dans la biologie de reproduction de l’Hirondelle rustique (Hirundo rustica). Nos Oiseaux 37, 101–116. RICHARDS, B. A. & GOODWIN, D. 1950. Swallow moulting remiges in Britain. British Birds 43, 300–301. RICKLEFS, R. E. 1965. Brood reduction in the curve-billed thrasher. Condor 67, 505–510. RICKLEFS, R. E. 1967. Relative growth, body constituents, and energy content of nestling Barn Swallows and Red-winged Blackbirds. Auk 84, 560–570. RICKLEFS, R. E. 1968a. Patterns of growth in birds. Ibis 110, 419–451. RICKLEFS, R. E. 1968b. Weight recession in nestling birds. Auk 85, 30–35. RIDGELY, R. S. & TUDOR, G. 1989. The Birds of South America. Volume 1. University of Texas Press, Austin. ROBERSON, D. 2002. Monterey Birds. Monterey Peninsula Audubon Society. ROBERTS, T. J. 1992. The Birds of Pakistan. Volume 2. Oxford University Press, Oxford. ROBERTSON, W. B. & WOOLFENDEN, G. E. 1992. Florida Bird Species. Florida Ornithological Society. ROBINSON, R. A. & SUTHERLAND, W. J. 2002. Post-war changes in arable farming and biodiversity in Great Britain. Journal of Applied Ecology 39, 157–176. ROBINSON, R. A., CRICK, H. Q. P. & PEACH, W. J. 2003. Population trends of Swallows Hirundo rustica breeding in Britain 1964–1998. Bird Study 50, 1–7. ROBSON, C. 2000. A Field-Guide to the Birds of South-East Asia. Princeton University Press, Princeton. ROSAIR, D. B. 1975. Swallows chasing bats. British Birds 68, 248. RÖSE, N. 2001. Zur Entwicklung der Brutbestände von Rauchschwalbe Hirundo rustica und Mehlschwalbe Delichon urbica in Oldisleben/Kyffhäuserkreis. Anzeiger des Veriens Thüringer Ornithologisches 4, 231–232. ROWAN M. K. 1968. The origins of European Swallows wintering in South Africa. Ostrich 39, 76–84. ROWAN, M. K. 1972. Winter quarters of Swallows. Bird Study 19, 54–55. ROWE, L. V., EVANS, M. R. & BUCHANAN, K. L. 2001. The function and evolution of the tail streamer in hirundines. Behavioral Ecology 12, 157–163. ROYAMA, T. 1969. A model for the global variation of clutch size in birds. Oikos 20, 562–567. RSPB 2004. Illegal bird hunting in southern Europe. www.rspb.org.uk/international/illegal_hunting

14639.qxd

24/1/06

236

3:54 pm

Page 236

Bibliography

RUBOLINI, D. & SCHIAVI, M. 2002. Tail length correlates with fat stores in pre-migratory roosting Barn Swallows Hirundo rustica. Ardea 90, 121–127. RUBOLINI, D., MASSI, A. & SPINA, F. 2002a. Replacement of body feathers is associated with low pre-migratory energy stores in a long-distance migratory bird, the Barn Swallow (Hirundo rustica). Journal of Zoology 258, 441–447. RUBOLINI, D., PASTOR, A. G., PILASTRO, A. & SPINA F. 2002b. Ecological barriers shaping fuel stores in Barn Swallows Hirundo rustica following the central and western Mediterranean flyways. Journal of Avian Biology 33, 15–22. RUDEBECK, G. 1955. Some observations at a roost of European Swallows and other birds in the southeastern Transvaal. Ibis 97, 572–580. RUGE, K. 1974. Europäische Schwalbenkatastrophe im Oktober1974. Vogelwarte 27, 299–300. RÜPPELL, W. 1934. Versuche zur Ortstreue und Fernorientierung der Vögel III. Vogelzug 5, 161–166. SACCHI, R., SAINO, N. & GALEOTTI, P. 2002. Features of begging calls reveal general condition and need of food of Barn Swallow (Hirundo rustica) nestlings. Behavioral Ecology 13, 268–273. SAFRAN, R. J. 2004. Adaptive site selection rules and variation in group size of Barn Swallows: individual decisions predict population patterns. American Naturalist 164, 121–131. SAFRAN, R. J. 2005. Individuals to Populations: Female Habitat- and Mate-selection Decisions and Group Size Variation in Barn Swallows. Ph.D. thesis, Cornell University. SAFRAN, R. J. & McGRAW, K. J. 2004. Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American Barn Swallows. Behavioral Ecology 15, 455–461. SAFRAN, R. J., NEUMAN, C. R., McGRAW, K. J. & LOVETTE, I. J. 2005. Dynamic paternity allocation as a function of male plumage color in Barn Swallows. Science 309, 2210–2212. SAINO, N. & MØLLER, A. P. 1994. Secondary sexual characters, parasites and testosterone in the Barn Swallow, Hirundo rustica. Animal Behaviour 48, 1325–1333. SAINO, N. & MØLLER, A. P. 1995a. Testosterone correlates of mate guarding, singing and aggressive behaviour in male Barn Swallows, Hirundo rustica. Animal Behaviour 49, 465–472. SAINO, N. & MØLLER, A. P. 1995b. Testosterone-induced depression of male parental behavior in the Barn Swallow: female compensation and effects of seasonal fitness. Behavioral Ecology and Sociobiology 36, 151–157. SAINO, N. & MØLLER, A. P. 1996. Sexual ornamentation and immunocompetence in the Barn Swallow. Behavioral Ecology 7, 227–232. SAINO, N., MØLLER, A. P. & BOLZERN, A.M. 1995. Testosterone effects on the immune system and parasite infestations in the Barn Swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behavioral Ecology 6, 397–404. SAINO, N., GALEOTTI, P., SACCHI, R. & MØLLER, A. P. 1997a. Song and immunological condition in male Barn Swallows (Hirundo rustica). Behavioral Ecology 8, 364–371. SAINO, N. BOLZERN, A. M. & MØLLER, A. P. 1997b. Immunocompetence, ornamentation, and viability of male Barn Swallows (Hirundo rustica). Proceedings of the National Academy of Sciences USA 94, 549–552. SAINO, N., CUERVO, J. J., NINNI, P., DE LOPE, F. & MØLLER, A. P. 1997c. Haematocrit correlates with tail ornament size in three populations of the Barn Swallow (Hirundo rustica). Functional Ecology 11, 604–610. SAINO, N, CUERVO, J. J., KRIVACEK, M., DE LOPE, F & MØLLER, A. P. 1997d. Experimental

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 237

237

manipulation of tail ornament size affects the hematocrit of male Barn Swallows (Hirundo rustica). Oecologia 110, 186–190. SAINO, N., PRIMMER, C. R., ELLEGREN, H. & MØLLER, A. P. 1997e. An experimental study of paternity and tail ornamentation in the Barn Swallow (Hirundo rustica). Evolution 51, 562–570. SAINO, N., CALZA, S. & MØLLER, A. P. 1997f. Immunocompetence of nestling Barn Swallows in relation to brood size and parental effort. Journal of Animal Ecology 66, 827–836. SAINO, N., CALZA, S. & MØLLER, A. P. 1998. Effects of a dipteran ectoparasite on immune response and growth trade-offs in Barn Swallow, Hirundo rustica, nestlings. Oikos 81, 217–228. SAINO, N., ELLEGREN, H. & MØLLER, A. P. 1999a. No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in Barn Swallows. Molecular Ecology 8, 399–406. SAINO, N., CALZA, S., NINNI, P. & MØLLER, A. P. 1999b. Barn Swallows trade survival against offspring condition and immunocompetence. Journal of Animal Ecology 68, 999–1009. SAINO, N., PRIMMER, C. R., ELLEGREN, H. & MØLLER, A. P. 1999c. Breeding synchrony and paternity in the Barn Swallow (Hirundo rustica). Behavioral Ecology and Sociobiology 45, 211–218. SAINO, N., STRADI, R., NINNI, P., PINI, E. & MØLLER, A. P. 1999d. Carotenoid plasma concentration, immune profile, and plumage ornamentation of male Barn Swallows (Hirundo rustica). American Naturalist 154, 441–448. SAINO, N., NINNI, P., CALZA, S., MARTINELLI, R., DE BERNARDI, F. & MØLLER, A. P. 2000a. Better red than dead: carotenoid-based mouth coloration reveals infection in Barn Swallow nestlings. Proceedings of the Royal Society of London B 267, 57–61. SAINO, N., NINNI, P., INCAGLI, M., CALZA, S., SACCHI, R. & MØLLER, A. P. 2000b. Begging and parental care in relation to offspring need and condition in the Barn Swallow (Hirundo rustica). American Naturalist 156, 637–649. SAINO, N., INCAGLI, M., MARTINELLI, R., AMBROSINI, R. & MØLLER, A. P. 2001a. Immunity, growth and begging behaviour of nestling Barn Swallows Hirundo rustica in relation to hatching order. Journal of Avian Biology 32, 263–270. SAINO, N., MARTINELLI, R. & MØLLER, A. P. 2001b. Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female Barn Swallows (Hirundo rustica). Journal of Evolutionary Biology 14, 95–109. SAINO, N., FERRARI, R.P., MARTINELLI, R., ROMANO, M., RUBOLINI, D. & MØLLER, A. P. 2002a. Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proceedings of the Royal Society of London B, 269, 1005–1009. SAINO, N., BERTACCHE, V., FERRARI, R. P., MARTINELLI, R., MØLLER, A. P. & STRADI, R. 2002b. Carotenoid concentration in Barn Swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proceedings of the Royal Society of London B 269, 1729–1733. SAINO, N., DALL’ARA, P., MARTINELLI R. & MØLLER, A. P. 2002c. Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the Barn Swallow. Journal of Evolutionary Biology 15, 735–743. SAINO, N., INCAGLI, M., MARTINELLI R. & MØLLER, A. P. 2002d. Immune response of male Barn Swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behavioral Ecology 13, 169–174. SAINO, N., AMBROSINI, R., MARTINELLI, R., CALZA, S., MØLLER, A. P. & PILASTRO, A. 2002e. Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the Barn Swallow. Molecular Ecology 11, 1533–1544.

14639.qxd

24/1/06

238

3:54 pm

Page 238

Bibliography

SAINO, N., AMBROSINI, R., MARTINELLI, R. & MØLLER, A. P. 2002f. Mate fidelity, senescence in breeding performance and reproductive trade-offs in the Barn Swallow. Journal of Animal Ecology 71, 309–319. SAINO, N., FERRARI, R. P., ROMANO, M., AMBROSINI, R. & MØLLER, A. P. 2002g. Ectoparasites and reproductive trade-offs in the Barn Swallow (Hirundo rustica). Oecologia 133, 139–145. SAINO, N., GALEOTTI, P., SACCHI, R., BONCORAGLIO, G., MARTINELLI R. & MØLLER, A. P. 2003a. Sex differences in begging vocalizations of nestling Barn Swallows, Hirundo rustica. Animal Behaviour 66, 1003–1010. SAINO, N., AMBROSINI, R., MARTINELLI, R., NINNI, P. & MØLLER, A. P. 2003b. Gape coloration reliably reflects immunocompetence of Barn Swallow (Hirundo rustica) nestlings. Behavioral Ecology 14, 16–22. SAINO, N., SUFFRITTI, C., MARTINELLI R., RUBOLINI, D. & MØLLER, A. P. 2003c. Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling Barn Swallows (Hirundo rustica). Behavioral Ecology 14, 318–325. SAINO, N., FERRARI, R.P., ROMANO, M., RUBOLINI, D. & MØLLER, A. P. 2003d. Humoral immune response in relation to senescence, sex and sexual ornamentation in the Barn Swallow (Hirundo rustica). Journal of Evolutionary Biology 16, 1127–1134. SAINO, N., FERRARI, R.P., ROMANO, M., MARTINELLI, R. & MØLLER, A. P. 2003e. Experimental manipulation of egg carotenoids affects immunity of Barn Swallow nestlings. Proceedings of the Royal Society of London B 270, 2485–2489. SAINO, N., ROMANO, M., SACCHI, R., NINNI, P., GALEOTTI, P. & MØLLER, A. P. 2003f. Do male Barn Swallows (Hirundo rustica) experience a trade-off between the expression of multiple sexual signals? Behavioral Ecology and Sociobiology 54, 465–471. SAINO, N., MARTINELLI, R., ROMANO, M. & MØLLER, A. P. 2003g. High heritable variation of a male secondary sexual character revealed by extra-pair fertilization in the Barn Swallow. Italian Journal of Zoology 70, 167–174. SAINO, N., ROMANO, M., FERRARI, R.P., MARTINELLI, R. & MØLLER, A. P. 2003h. Maternal antibodies but not carotenoids in Barn Swallow eggs covary with embryo sex. Journal of Evolutionary Biology 16, 516–522. SAINO, N., SZÉP, T., ROMANO, M., RUBOLINI, D., SPINA, F. & MØLLER, A. P. 2004a. Ecological conditions during winter predict arrival date at the breeding quarters in a trans-Saharan migratory bird. Ecology Letters 7, 21–25. SAINO, N., ROMANO, M., AMBROSINI, R., FERRARI, R.P. & MØLLER, A. P. 2004b. Timing of reproduction and egg quality covary with temperature in the insectivorous Barn Swallow, Hirundo rustica. Functional Ecology 18, 50–57. SAINO, N., SZÉP, T., AMBROSINI, R., ROMANO, M. & MØLLER, A. P. 2004c. Ecological conditions during winter affect sexual selection and breeding in a migratory bird. Proceedings of the Royal Society of London B 271, 681–686. SAMUEL, D. E. 1969. The Ecology, Behavior, and Vocalizations of Sympatric Barn and Cliff Swallows in West Virginia. Ph.D. thesis, West Virginia University. SAMUEL, D. E. 1971a. Vocal repertoires of sympatric Barn and Cliff Swallows. Auk 88, 839–855. SAMUEL, D. E. 1971b. The breeding biology of Barn and Cliff Swallows in West Virginia. Wilson Bulletin 83, 284–301.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 239

239

SAUER, J. R., HINES, J. E. & FALLON, J. 2004. The North American Breeding Bird Survey. Results and Analysis 1966–2003. Version 2004.1. USGS Patuxent Wildlife Research Center, Laurel, Maryland. SAUROLA, P. 2000. Summary: the EURING Swallow Project in Finland in 1999. Linnut-vuosikirja. 1999, 57–66. SAUROLA, P. 2001. Summary: the EURING Swallow Project in Finland in 2000. Linnut-vuosikirja. 2000, 82–90. SAUROLA, P. 2003. Summary: the EURING Swallow Project in Finland in 2002. Linnut-vuosikirja. 2002, 103–108. SAUSSAY, M. 1993a. Un cas de ‘choix’ de l’emplacement du nid pour la premierè et la seconde couvée d’hirondelles de cheminée. Cormoran 8, 240–242. SAUSSAY, M. 1993b. Un traumatisme important subi par la femelle n’empeche pas un couple d’hirondelle de cheminée (Hirundo rustica) de mener à bien sa nichée. Cormoran 8, 307–308. SAUSSAY, M. & JACOB, C. 1993. Un cas de bigamie chez l’hirondelle de cheminée Hirundo rustica. Cormoran 9, 73–74. SCHIFFERLI, L., SCHIFFERLI, A. & BLUM, H. 1984. Brutverbreitung von Mauersegler Apus apus, Mehlschwalbe Delichon urbica und Rauchschwalbe Hirundo rustica im Kanton Tessin und im Misox GR. Ornithologische Beobachter 81, 215–225. SCHMID, H., LUDER, R. NAEF-DAENZER, B., GRAF, R. & ZBINDEN, N. 1998. Atlas des Oiseaux Nicheurs de Suisse. Distribution des Oiseaux Nicheurs en Suisse et Lichtenstein en 1993–1996. Station Ornithologique Suisse, Sempach. SCHODDE, R. & MASON, I. J. 1999. The Directory of Australian Birds: Passerines. CSIRO, Canberra. SCHULZE-HAGEN, K. 1969. Beobachtungen an der Rauchschwalbe (Hirundo rustica). Charadrius 5, 22–26. SCHULZE-HAGEN, K. 1970. Ein Beitrag zur Ernährung der Rauchschwalbe (Hirundo rustica). Charadrius 6, 81–90. SCHWILCH, R., GRATTAROLA, A., SPINA, F. & JENNI, L. 2002. Protein loss during long-distance migratory flight in passerine birds: adaptation and constraint. Journal of Experimental Biology 205, 687–695. SEXTON, D. 1992. Black holes of Kuwait. Birding in SA 44, 68–69. SHELDON, B. C. 2000. Differential allocation: tests, mechanisms and implications. Trends in Ecology and Evolution, 15 397–402. SHELDON, F. H. & GILL, F. B. 1996. A reconsideration of songbird phylogeny, with emphasis on the evolution of titmice and their sylvioid relatives. Systematic Biology 45, 473–495. SHELDON, F. H. & WINKLER, D. W. 1993. Intergeneric phylogenetic relationships of swallows estimated by DNA-DNA hybridization. Auk 110, 798–824. SHELDON, F. H., WHITTINGHAM, L. A. & WINKLER, D. W. 1999. A comparison of cytochrome b and DNA hybridization data bearing on the phylogeny of swallows (Aves: Hirundinidae). Molecular Phylogenetics and Evolution 11, 320–331. SHELDON, F.H., WHITTINGHAM, L.A., MOYLE, R.G., SLIKAS, B. & WINKLER, D.W. 2005. Phylogeny of swallows (Aves: Hirundinidae) estimated from nuclear and mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 35, 254–270. SHIELDS, W. M. 1984a. Factors affecting nest and site fidelity in Adirondack Barn Swallows (Hirundo rustica). Auk 101, 780–789.

14639.qxd

24/1/06

240

3:54 pm

Page 240

Bibliography

SHIELDS, W. M. 1984b. Barn Swallow mobbing: self-defence, collateral kin defence, group defence, or parental care? Animal Behaviour 32, 132–148. SHIELDS, W. M. & CROOK, J. R. 1987. Barn Swallow coloniality: a net cost for group breeding in the Adirondacks? Ecology 68, 1373–1386. SHIELDS, W. M., CROOK, J. R., HEBBLETHWAITE, M. L. & WILES-EHMANN, S. S. 1988. Ideal free coloniality in the swallows. In Slobodchikoff, C. N. (ed.), The Ecology of Social Behavior, pp. 189–228. Academic Press, San Diego. SHIRIHAI, H. 1996. The Birds of Israel. Academic Press, London. SHYKOFF, J. A. & MØLLER, A. P. 1999. Fitness and asymmetry under different environmental conditions in the Barn Swallow. Oikos 86, 152–158. SKEAD, D. M. & SKEAD, C. J. 1970. Hirundinid mortality during adverse weather, November 1968. Ostrich 41, 247–251. SIRIWARDENA, G. M., BAILLIE, S. R. & WILSON, J. D. 1998a. Variation in the survival rates of some British passerines with respect to their population trends on farmland. Bird Study 45, 276–292. SIRIWARDENA, G. M., BAILLIE, S. R., BUCKLAND, S. T., FEWSTER, R. M., MARCHANT, J. H. & WILSON, J. D. 1998b. Trends in the abundance of farmland birds: a quantitative comparison of smoothed Common Bird Census indices. Journal of Applied Ecology 35, 24–43. SLAGSVOLD, T., SANDVIK, J., ROFSTAD, G., LORENTSEN, O. & HUSBY, M. 1984. On the adaptive value of intraclutch egg-size variation in birds. Auk 101, 685–697. SLUD, P. 1964. The birds of Costa Rica. Bulletin of the American Museum of Natural History, 128. SMIRENSKY, S. M. & MISHCHENKO, A. L. 1981. [Taxonomical status and history of formation of the range of Hirundo rustica in the Amur Territory]. Zoologicheskiıˇ Zhurnal 60, 1533–1541 [in Russian]. SMITH, H. G. & MONTGOMERIE, R. 1991. Sexual selection and the tail ornaments of North American Barn Swallows. Behavioral Ecology and Sociobiology 28, 195–201. SMITH, H. G. & MONTGOMERIE, R. 1992. Male incubation in Barn Swallows: the influence of nest temperature and sexual selection. Condor 94, 750–759. SMITH, H. G., MONTGOMERIE, R., PÕLDMAA, T., WHITE, B. N. & BOAG, P. T. 1991. DNA fingerprinting reveals relation between tail ornaments and cuckoldry in Barn Swallows, Hirundo rustica. Behavioral Ecology 2, 90–98. SMITH, M. J. & GRAVES, H. B. 1978. Some factors influencing mobbing behavior in Barn Swallows (Hirundo rustica). Behavioral Biology 23, 355–372. SMOGORZHEVSKY, L. A. & KOTKOVA, L. I. 1973.[ Characteristics of nestlings’ nutrition in some species of insectivorous synantropic birds.] Vestnick Zoologi 3, 34–39 [in Russian]. SNAPE, J. 2002. Mud carrying by House Martins and Barn Swallows. British Birds 95, 654. SNAPP, B. D. 1973. The Occurrence of Colonial Breeding in the Barn Swallow (Hirundo rustica) and its Adaptive Significance. Ph.D thesis, Cornell University. SNAPP, B. D. 1976. Colonial breeding in the Barn Swallow (Hirundo rustica) and its adaptive significance. Condor 78, 471–480. SÖDERSTRÖM, B. & PÄRT, T. 2000. Influence of landscape scale on farmland birds breeding in seminatural pastures. Conservation Biology 14, 522–533. SOKOLOV, L. V., MARKOVETS, M. Y., SHAPOVAL, A. P. & MOROZOV, Y. G. 1998. Long-term trends in the timing of spring migration of passerines on the Courish spit of the Baltic Sea. Avian Ecology and Behaviour 1, 1–21.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 241

241

SOLER, J. J., CUERVO, J. J., MØLLER, A. P. & DE LOPE, F. 1998. Nest building is a sexually selected behaviour in the Barn Swallow. Animal Behaviour 56, 1435–1442. SPARKS, T. H. & BRASLAVSKÁ, O. 2001. The effects of temperature, altitude and latitude on the arrival and departure dates of the Swallow Hirundo rustica in the Slovak Republic. International Journal of Biometeorology 45, 212–216. SPARKS, T. H. & CAREY, P. D. 1995. The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. Journal of Ecology 83, 321–329. SPARKS, T. H. & LOXTON, R. G. 2003. Indicators of climate change in the UK. 29. Arrival date of the Swallow. http://www.edinburgh.ceh.ac.uk/iccuk/indicators/29.htm SPARKS, T. H., HAYEN, H., BRASLAVSKÁ, O. & LEHIKOINEN, E. 1999. Are European birds migrating earlier? BTO News 223, 8–9. SPARKS, T. H., ROBERTS, D. R. & CRICK, H. Q. P. 2001. What is the value of first arrival dates of spring migrants in phenology? Avian Ecology and Behaviour 7, 75–85. SPEICH, S. M., JONES, H. L. & BENEDICT, E. M. 1986. Review of the natural nesting of the Barn Swallow in North America. American Midland Naturalist 115, 248–254. SPENCER, K. A. & BRYANT, D. M. 2002. State-dependent behaviour in breeding Barn Swallows (Hirundo rustica): consequences for reproductive effort. Proceedings of the Royal Society of London B 269, 403–410. SPINA, F., MASSI, A. & MONTEMAGGIORI, A. 1994. Back from Africa: who’s running ahead? Differential migration of sex and age classes in Palaearctic-African spring migrants. Ostrich 65, 137–150. STENNING, M. J. 1996. Hatching asynchrony, brood reduction and other rapidly reproducing hypotheses. Trends in Ecology and Evolution 11, 243–246. STEVENSON, H. M. 1978. Barn Swallows nesting in the interior of the Florida Panhandle. Florida Field Naturalist 6 , 27–29. STEVENSON, I. R. & BRYANT, D. M. 2000. Climate change and constraints on breeding. Nature 406, 366–367. STOLESON, S. H. & BEISSINGER, S. R. 1999. Egg viability as a constraint on hatching asynchrony at high ambient temperatures. Journal of Animal Ecology 68, 951–962. STONER, D. 1935. Temperature and growth studies on the Barn Swallow. Auk 52, 400–407. STRESEMANN, E. & STRESEMANN, V. 1968. Im Sommer mausernde Populationen der Rauchschwalbe, Hirundo rustica. Journal für Ornithologie 109, 475–484. SUZUKI, H. 1998. [The breeding status of the Barn Swallow Hirundo rustica at Yahata River mouth, Hiroshima.] Strix, 16, 99–108 [in Japanese]. SWADDLE, J. P. & CUTHILL, I. C. 1994. Female zebra finches prefer males with symmetric chest plumage. Proceedings of the Royal Society of London B 258, 267–271. SWARTH, H. S. 1935. A Barn Swallow’s nest on a moving train. Condor 37, 84–85. SZÉP, T. & MØLLER, A. P. 2005. Using remote sensing data to identify migration and wintering areas, and to analyze effects of environmental conditions on migratory birds. In Greenberg, R. & Marra, P. (eds), Birds of Two Worlds: the Ecology and Evolution of Migratory Birds. Johns Hopkins University Press, Baltimore. TAYLOR, L. R. 1963. Analysis of the effect of temperature on insects in flight. Journal of Animal Ecology 32, 99–117.

14639.qxd

24/1/06

242

3:54 pm

Page 242

Bibliography

THELLESEN, P. V. 2000. Bestanden af Lansvale Hirundo rustica pa en gard i Hjortkaer i Sydvestjylland 1971–1998. Dansk Ornitologisk Forenings Tidsskrift 94, 5–11. THOMAS, A. L. R. 1993a. On the aerodynamics of birds’ tails. Philosophical Transactions of the Royal Society of London B 340, 361–380. THOMAS, A. L. R. 1993b. The aerodynamic costs of asymmetry in the wings and tail of birds: asymmetric birds can’t fly around tight corners. Proceedings of the Royal Society of London B 254, 181–189. THOMAS, A. L. R. 1996a. The flight of birds that have wings and a tail: variable geometry expands the envelope of flight performance. Journal of Theoretical Biology 183, 237–245. THOMAS, A. L. R. 1996b. Why do birds have tails? The tail as a drag reducing flap and trim control. Journal of Theoretical Biology 183, 247–253. THOMAS, A. L. R. & BALMFORD, A. 1995. How natural selection shapes birds’ tails. American Naturalist 146, 848–868. THOMAS, A. L. R. & ROWE, L. 1997. Experimental tests on tail elongation and sexual selection in Swallows (Hirundo rustica) do not affect the tail streamer and cannot test its function. Behavioral Ecology 8, 580–581. THOMAS, J. F. 1933–1939. Food of nestling Swallows. British Birds 27, 231–232, 28, 171–172, 29, 244–245, 30, 293–294, 31, 234–235, 32, 133–136. THOMPSON, B. C. 1990. Behaviour of Swallows with feather. British Birds 83, 239. THOMPSON, M. L. P. 1992. Reproductive Success and Survival of Swallows Hirundo rustica: Effects of Age and Breeding Condition. Ph.D. thesis, University of Stirling TIAINEN, J., PEKKALA, T., PIIROINEN, J., VICKHOLM, M. & VIROLAINEN, E. 1985. [Changes in the avifauna of farmland at Lammi, southern Finland during the past 50 years.] Lintumies, 20, 30–42 [in Finnish]. TRYJANOWSKI, P., KUZ´NIAK, S. & SPARKS, T. 2002. Earlier arrival of some farmland migrants in western Poland. Ibis 144, 62–68. TUCKER, G. M. & HEATH, M. F. 1994. Birds in Europe. Their Conservation Status. BirdLife International, Cambridge. TURNER, A. K. 1980. The Use of Time and Energy by Aerial Feeding Birds. Ph.D. thesis, University of Stirling. TURNER, A. K. 1981. Lepidopteran larvae in the diet of the swallow. Bird Study 28, 65. TURNER, A. K. 1982a. Optimal foraging by the Swallow (Hirundo rustica, L.): prey size selection. Animal Behaviour 30, 862–872. TURNER, A. K. 1982b. Timing of laying by Swallows (Hirundo rustica) and Sand Martins (Riparia riparia). Journal of Animal Ecology 51, 29–46. TURNER, A. K. 1983. Time and energy constraints on the brood size of Swallows, Hirundo rustica, and Sand Martins, Riparia riparia. Oecologia 59, 331–338. TURNER, A. K. 2004. Family Hirundinidae (Swallows and Martins). In del Hoyo, J., Elliott, A. & Christie, D. A. (eds), Handbook of the Birds of the World. Volume 9, pp. 602–685. Lynx Edicions, Barcelona. TURNER, A. K. & BRYANT, D. M. 1979. Growth of nestling sand martins. Bird Study 26, 117–122. TURNER, L. M. 1886. Contributions to the Natural History of Alaska. US Government Printing Office, Washington.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 243

243

UCHIDA, S. 1932. Studies of Swallows by the banding method. Bird-banding 3, 1–11. VAISÄNEN, R. A., LAMMI, E. & KOSKIMIES, E. 1998. Distribution, Numbers and Population Changes of Finnish Breeding Birds. Otava, Keuruu. VAN DEN BRINK, B. 1994. Juvenile Barn Swallow moulting flight-feathers in July in the Netherlands. Dutch Birding, 16, 18–19. VAN DEN BRINK, B. 1997. European Swallows Hirundo rustica in Botswana. Babbler 32, 32–33. VAN DEN BRINK, D. 2003. Hygiënemaatregelen op moderne boerenbedrijven en het lot van boerenzwaluwen Hirundo rustica. Limosa 76, 109–116. VAN DEN BRINK, B. & VAN DER HAVE, T. M. 1993. Swallow ringing in the Netherlands and southern Africa: the Botswana Swallow Project. Safring News 22, 27–30. VAN DEN BRINK, B., BIJLSMA, R G. & VAN DER HAVE, T. M. 1997. European Swallows Hirundo rustica in Botswana. WIWO Report 56, Zeist, The Netherlands. VAN DEN BRINK, B., BIJLSMA, R. G. & VAN DER HAVE, T. M. 1998. European songbirds and Barn Swallows Hirundo rustica in Ghana. WIWO report 58, Zeist, The Netherlands. VAN DEN BRINK, B., BIJLSMA, R. G. & VAN DER HAVE, T. M. 2000. European Swallows Hirundo rustica in Botswana during three non-breeding seasons: the effects of rainfall on moult. Ostrich 71, 198–204. VAN DEN BRINK, B., VAN DEN BERG, A. & DEUZEMAN, S. 2003. Trapping Barn Swallows Hirundo rustica roosting in Botswana in 2003. Babbler 43, 6–14. VAN DER HAVE, T. M. & VAN DEN BRINK, B. 1999. Barn Swallows in Africa: effects of rainfall on body condition and speed of moult. In Adams, N. J. & Slotow, R. H. (eds), Proceedings of the 22nd International Ornithological Congress, Durban, p. 229. Birdlife South Africa, Johannesburg. VAN EE, C. A. 1988. Stomach contents: European Swallow (Hirundo rustica). Mirafra 5, 27. VAN JAARSVELD, A. S. & CHOWN, S. L. 2001. Climate change and its impacts in South Africa. Trends in Ecology and Evolution 16, 13–14. VANSTEENWEGEN, C. 1981. Nidification d’un hybride presume entre l’hirondelle de fenêtre (Delichon urbica) et l’hirondelle de cheminée (Hirundo rustica). Gerfaut 71, 611–615. VANSTEENWEGEN, C. 1982. Longévité et structure des nids d’hirondelle de cheminée. Aves 19, 247–251. VANSTEENWEGEN, C. 1988. Choix de l’habitat, fidelité et répartition spatiale chez l’hirondelle de cheminée. Alauda 56, 350–364. VANSTEENWEGEN, C. 1992. Étude de passage et des retours de l’hirondelle de cheminée Hirundo rustica en Belgique. Aves 29, 155–176. VAN VLECK, R. 2004. Artificial barn swallow nests. http://www.americanartifacts.com/smma/per/ b4info.htm VERDOORN, G. H. 1999. Solving the problems of pesticide misuse for avian conservation in southern Africa. In Adams, N. J. & Slotow, R. H. (eds), Proceedings of the 22nd International Ornithological Congress, Durban, pp. 1033–1042. BirdLife International, Johannesburg. VEROMANN, H. 1981. Air temperature during the arrival of the Swallow in Estonia in the years 1965–1974. Communications of the Baltic Commission for the Study of Bird Migration 3, 79. VICKERY, J. A., TALLOWIN, J. R., FEBER, R.E., ASTERAKI, E. J., ATKINSON, P. W., FULLER, R. J. & BROWN, V. K. 2001. The management of lowland neutral grasslands in Britain: effects of agricultural practices on birds and their food resources. Journal of Applied Ecology 38, 647–664. VON VIETINGHOFF-RIESCH, A. 1955. Die Rauchschwalbe. Duncker & Humblot, Berlin.

14639.qxd

24/1/06

244

3:54 pm

Page 244

Bibliography

WABC-TV 2004. Birds learn to operate automatic doors. http://abclocal.go.com/wabc/features/ strangenews/wabc_061604_birds.html 16 June. WAKELING, D. 1977. European Swallows shopping at Westguide. Honeyguide 43, 171–172. WANG, S.-M. 1959. Preliminary studies on the life history of the House Swallow. Acta Zoologica Sinica 11, 138–144. WARD, P. & ZAHAVI, A. 1973. The importance of certain assemblages of birds as ‘information-centres’ for food finding. Ibis 115, 517–534. WARD. S. 1992. Energetics of Laying and Incubation in Birds: Studies of Swallows Hirundo rustica, Dippers Cinclus cinclus and Japanese Quail Coturnix coturnix japonica. Ph.D. thesis, University of Stirling. WARD, S. 1995. Causes and consequences of egg size variation in Swallows Hirundo rustica. Avocetta 19, 201–208. WARD, S. 1996. Energy expenditure of female Barn Swallows Hirundo rustica during egg formation. Physiological Zoology 69, 930–951. WARD, S. & BRYANT, D. M. 2006. Barn Swallows Hirundo rustica form eggs mainly from current intake. Journal of Avian Biology, in press. WARRICK, D. R. 1998. The turning and linear-maneuvring performance of birds: the cost of efficiency for coursing insectivores. Canadian Journal of Zoology 76, 1063–1079. WATSON, A. & RAE, R. 1998. Use by birds of rape fields in east Scotland. British Birds 91, 144–145. WAUGH, D. R. 1978. Predation Strategies in Aerial Feeding Birds. Ph.D. thesis, Stirling University. WAUGH, D. R. & HAILS, C. J. 1983. Foraging ecology of a tropical aerial feeding bird guild. Ibis 125, 200–217. WEATHERHEAD, P. J., SEALY, S. G. & BARCLAY, R. M. R. 1985. Risks of clustering in thermally-stressed Swallows. Condor 87, 443–444. WEGGLER, M. & WIDMER, M. 2000. Vergleich der Brutvogelbestände im Kanton Zürich 1986–1988 und 1999. Ornithologische Beobachter 97, 223–232. WEISHEIT, A. S. & CREIGHTON, P. D. 1989. Interference in house sparrows in nesting activities of Barn Swallows. Journal of Field Ornithology 60, 323–328. WELLBOURN, M. 1993. Aspects of the Breeding Biology of a Swallow Hirundo rustica Population. Ph.D. thesis, Manchester University. WESTERTERP, K. R. & BRYANT, D. M. 1984. Energetics of free existence in swallows and martins (Hirundinidae) during breeding: a comparative study using doubly labeled water. Oecologia 62, 376–381. WHITE, F. N. & KINNEY, J. L. 1974. Avian incubation. Science 186, 107–115. WHITE, G. 1789. The Natural History and Antiquities of Selbourne. B. White & Son, London. WHITE, W. W. 1941. Bird of first brood of Swallow assisting to feed second brood. British Birds 34, 179. WHITFORD, P. C. 1995. Albino Barn Swallow in Winona County. Loon 67, 253. WHITMORE, R. C., MOSHER, J. A. & FROST, H. H. 1977. Spring migrant mortality during unseasonable weather. Auk 94, 778–781. WILDE, N. A. J. 1992. Swallows feeding live honeybees to their young. British Birds 85, 616. WINDIG, J. J. & FLORUS, M. 1997. Evolutie van het broedbestand in Vlaanderen van Oeverswaluw Riparia riparia, Huiszwaluw Delichon urbica en Boerenzwaluw Hirundo rustica. Oriolus 63, 1–32.

14639.qxd

24/1/06

Bibliography

3:54 pm

Page 245

245

WINKLER, D. W. & McCARTY, J. P. 1990. Method for transplanting nests of Barn Swallows. Journal of Field Ornithology 61, 426–430. WINKLER, D. W. & SHELDON, F. H. 1993. The evolution of nest construction in swallows (Hirundinidae): a molecular phylogenetic perspective. Proceedings of the National Academy of Sciences, USA 90, 5705–5707. WITHGOW, J. H. & McMAHON, J. A. 1993. Conspecific harassment of a leucistic Barn Swallow. Bulletin of the Oklahoma Ornithological Society 26, 38–39. WOLFE, D. H. 1994. Brown-headed Cowbirds fledged from Barn Swallow and American Robin nests. Wilson Bulletin 106, 764–766. WOOD, H. B. 1937. Observations at a Barn Swallow’s nest. Wilson Bulletin 96, 96–100. WRIGHT, J. 1992. Certainty of paternity and paternal care. Animal Behaviour 44, 380–381. YEATMAN-BERTHELOT, D. 1991. Atlas des Oiseaux de France en hiver. Société Ornithologique de France. YOUNG, G. H. E. 1974. Cuckoo parasitizing Swallow. British Birds 67, 478. YTREBERG, N. J. 1986. The behaviour of the House Martin Delichon urbica and the Barn Swallow Hirundo rustica in the incubation period during a spell of adverse weather. Fauna norvegica Series C Cinclus 9, 35–48. YUNICK, R. P. 1977. A Caribbean Barn Swallow recovery. Auk 94, 149–150. ZABASHTA, A. V. 2000. [Biology of the Barn Swallow.] Caucasian Ornithological Bulletin, 12, 68–72 [in Russian] ZAHAVI, A. 1975. Mate selection: a selection for a handicap. Journal of Theoretical Biology 53, 205–214. ZIELIN´SKI, P. & BAN´BURA, J. 1995. Selfish behaviour of juvenile Barn Swallows (Hirundo rustica) intruding in active nests. Ornis Fennica 72, 89–90 ZIELIN´SKI, P. & BAN´BURA, J. 1998. Egg size variation in the Barn Swallow Hirundo rustica. Acta Ornithologica 33, 191–196. ZIELIN´SKI, P. & WOJCIECHOWSKI, Z. 1999. Feeding frequency in the Barn Swallow Hirundo rustica in relation to time of the day. Acta Ornithologica 34, 85–88. ZINK, R. M., ROHWER, S., ANDREEV, A. V. & DITTMANN, D. L. 1995. Trans-Beringia comparisons of mitochondrial DNA differentiation in birds. Condor 97, 639–649.

14639.qxd

24/1/06

3:54 pm

Page 246

14639.qxd

24/1/06

3:54 pm

Page 247

Index Page numbers for fi f gures and tables are in italic type. Acacia cyclops 37, 48 age 24–5, 63, 44, 63, brooding 94, 114, 142–3, 150–5 dispersal 195 mating 56, 70, 76 migration 182 productivity 115–120, 122–3, 133, 143–55 and size of clutch 25–6, 82, 138, 163–6 aggression 50–2, 61–4, 79, 96, 146, 196 agricultural intensification 53–4, 106, 132, 197, 204–8 agri-environment schemes 205 agrochemicals see Fertilisers; Pesticides alarm call see calls albinism 23, 80 Algeria 17, 26, 171, 184, 201 altitude 51, 177–8, 192, feeding 28–9, 45, 49, 99–100, 129, 184–5 androgens 63, 81, 118, 134 anti-predator behaviour 41, 47, 55, 91, 95, 103–4, 143–4 ants 36–8, 45–6, 161–2 aphids 28, 37–8, 43–5 arable crops 41, 44, 53, 99, 105–6, 197, 203–8 Argentina 22, 101, 174, 178, 201, 208 arrival dates 25, 48, 56, 69, 75 and breeding 108, 110–11, 113–4, 118 and chicks 134, 136, 169–71 and health 150, 153–5, 178–92 and mating 82–3, 86–8. 96, 118 Australia 17–20, 37, 174, 176, 180–6 bathing 50

bats 51, 158 bees 36, 40 beetles 36–8, 40, 43–6, 159 begging behaviour 16–17, 51, 54–7, 137–8 Belgium 173, 191, 193–4 bill size 17, 23, 26, 38–40 BirdLife International 169, 199–200 Blackbird, Eurasian 102, 210 blow flies 28, 38–40, 159 larvae 134 Bobcat 161, 211 body condition 26, 70–80, 84–7, 135–8, 147–8, productivity 152–3, 163–4, 192–3 females 45, 82–3, 114, 116–7 after laying 126–7, 146–8, 152–5, 160–1, 183–3 males 63, 69–76, 82, 94, 147–8, 163, 182 migration 170, 187, 192–3 body temperature 136, 170 Botswana 48–50, 73–4, 170–1, 173–4, 189, 191–2 breeding season 35–42, 45, 47–52, 60, 72, 82–3, 86 and nests 96–7, 99, 113–14, 118, 144, 156, 201–2 breeding site fidelity 19, 57–9, 52, 55–9, 83, 85–7 and nests 96–7, 201–2 breeding success 55–8, 71–7, 81–3, 86, 96–7, and age 82–3, 94, 115, 139–43, 149–55, 182, 195–6 and habitat quality 96, 104–5, 116, 130–6, 155–6, 162, and nest 105, 110, 136–49, 150–2, 157, 160, 201

14639.qxd

24/1/06

3:54 pm

Page 248

248 and weather 41–2, 54–5, 75, 82, 108–10, 122–3, 149–6, migration 168, 182, 202–3, 208 lifetime 83, 86, 97, 154–5 Britain 199, 157, 159, 169, migration 173, 175–81, 183–6, 191, 194–5, population 198, 200, 203–4, British Trust for Ornithology (BTO) 167, 187 brood parasitism by Barn Swallows, see egg-dumping by cuckoos and cowbirds 158 brood patch 24, 123 brood size 55, 57–8, 81–2, 87–9, 92–3, 118 chicks 121–3, 130, 132–7 productivity 147, 150–6, 160, 162–6 broods 52, 87, 90, 109–11, 113, 120–3, 124, chicks 134–6, 138–9, 142, productivity 150–6, 159, 161–5, 202 first 38, 48, 71, 73, 83, 87, 93, 96, 201 young 113, 117–22, 132, 142, 144–5, 150 second 28, 38, 42, 48, 78, 81–3, 87, 90 productivity 150–2, 153–6, 159, 202 young 114, 117–31, 132, 136, 144–5 third 77, 87, 113, 134, 150–1, 177 Bullfrog 168, 209 calcium 37–8 California 22, 70, 170, 175, 178, 201 calls 49, 59, 66, alarm 47, 51, 64–5, 89–91, 143–5 deceptive 91 begging 64–7. 137–8, 145 contact 50, 64–7, 137 copulation 64–5, 69, 85 distress 65 mate attraction 64, 69 sex differences 64–7 Canada 19–22, 24, 89, 92, 101–2 migration, population 175, 177, 201, 204 carotenoids 116–17, 137, 164 Cat 51, 161, 168–9, 144, 211 cattle 42–3, 46, 53–4, 57, 100, 104–6, 114 and productivity 156, 184–5, 204–8

The Barn Swallow dairy 53, 58, 105–6, 132, 135–6 and productivity 151–2, 155–6, 205–7 Central America 22, 24, 174, 184 Chernobyl 17, 23, 80, 157 chick-brooding 95–6, 136, 139, 144, 191 chick-feeding 27, 32–4, 37–46, 55, 64, 66 costs 77, 80–3, 89–90, 95 and nest 121–3, 130–48, 156 chicks 65–6, 129–48 development 106, 121–2, 130–2, 132–41 and parasites 23–5, 110, 117, 134–6, 142, 145, 155–61 and parental age 142–3, 150–6, 163 and weather 22–3, 117, 129–36, 141–2, 155–6 diet 22–3, 38–46, 77, 132, 135, 137, 147 growth rate 55, 118, 130–6, 144–5, 157, 160 immunocompetence 75, 117–18, 121–2, 134–6 and productivity 154–5, 157, 163 weight 20, 55, 115–18, 130–6, 153–4, 162–4, 160 weight hierarchy 116, 130, 162 China 16, 20, 173–4, 184, 191–2 climate change 114, 176–7, 181–2, 203 Chipmunk, Eastern 161, 211 clutch size 88, 92, 108, 118–20 constraints on 81–2, 115–116, 121–3, 154–6, 202 effects of parasites 63, 122, 125, 150–5, 159–6 effects of parental age 82, 94, 142–3, 150–5, 159–60 effects of weather 105, 109–18, 121–2, 156, 202 variation in 115–20, 121–7, 153 collisions with buildings and vehicles 168–9 Common Bird Census 200, 202 copulation 23, 63–4, 69–70, 76, 84, 92, 97 rate 32, 56. 63–4, 69, 70, 79, 85–92 corticosterone 73, 135 courtship 32, 64–5, 69–73, 193 Cowbird, Brown-headed 158, 210 Crow Common 161–2, 210 Large-billed 161–2, 210

14639.qxd

24/1/06

3:54 pm

Page 249

Index Cuckoo, Common 158, 210 Czech Republic 53–4, 99, 181, 207 daily energy expenditure 39–46, 146–8 dairy farming 53, 58, 105–6, 132, 135–6 and productivity 151–2, 155–6, 205–7 defence of offspring 33, 47, 51, 55, 95, 143–4 Denmark 16–17, 20–2, 24–6, 34, 38–9, 51–9 breeding 71, 73–4, 78–9, 84–90, 100–2, 104–6 chicks 134, 138, eggs 96, 114, 119–20 dispersal 193–4 juveniles 150–6, 159 migration 174, 180–4 population 198–9, 201–2 survival 78, 166–71 density dependence 53–9, 94, 120, 166, 168 and population 198, 204 deserts 19, 26, 171, 183–4, 189–90, 203 diet 36–40 adults 36–47, 194 chicks 40–6, 135, 140–3 prey size 34, 36–46, 48 dispersal 17 adult 51–4, 193–7 natal 162–3, 173, 193–6 distribution 16, 18–20 disturbance 115, 161–2 , 195 DNA analyses 22, 87 Dogwood, Red Osier 37, 209 Dormouse 161–2, 211 drought effect on breeding 109, 152, 156, 203 on migration 176, 178 in winter quarters 49–50, 170–1, 189, 192, 205 Ebakken-Boje 169 egg-dumping 56, 66, 87, 96 egg-ejection 56, 66, 96–7, 121, 158, 161 egg-laying 36, 42, 64, 76, 81, 96, 108–23, 153 interruptions 91, 100, 115, 118, 123–5

249 timing of 55–6, 69–70, 82, 85–92, 109–20 and survival 134, 152–5, 190, 202, 206 effect of weather 112–20, 202 eggs 56, 79, 115–18, 149, 161 coloration 106–7, 115 composition 116–17, 126, 155 desertion 115, 156, 161 quality 89, 116–17, 155 size 115–116, 127, 130 and weather 109, 113, 115–20, 123–5 weight 115–17 Egypt 20, 101, 174, 198 Elderberry 30, 57, 209 energetics 16, 30–3, 45, 146–8 of egg-laying 77, 79, 140–3, 189–93, 203 of incubation 114–17, 126–8, 146–7 of chick-rearing 15, 39–45, 105, 123, 132, 140–3 England 41, 99–100, 151, 156, 186, 204–06 and migration 173, 175, 177–80 Estonia 17, 54, 179, 198 Ethiopia 16, 19 European Union (EU) 169, 205, 207 European Union for Bird Ringing (EURING) Swallow Project 17, 22, 187 evolution 17–18, of tail 32–6 extra-pair chicks 23, 50, 86, 88–90 extra-pair copulation 23, 32, 50, 56 and choice of mate 68, 76, 81, 84–92, 146 extra-pair paternity 23, 70, 76, 81–2, 84–96, 155 faecal sacs 143 Falcons, Eleonora’s 168, 210 Lanner 168, 210 Peregrine 65, 168, 211 Red-necked 168, 211 fat deposition 122, 131, 141–8, 187–9, 202 fat stores 17, 23, 75, 83, 103 chicks 126–8, 130–2, 146–8, 170–1, and migration 188–9, 193

14639.qxd

24/1/06

3:54 pm

Page 250

250 feathers 51, 103, 107–8, 125, 145–6 and productivity 157, 159, 173, 176, 190–3 breakage 35–6, 77, 80, 193 care of 50 see also preening fault bars 77–8, 132 growth 26, 35, 77, 130–6, 144–5 survival 157, 190–3, 202 feeding 15–16, 30, 36, 104–8, 115, 185–6 of chicks 27, 32–4, 37–45, 64, 66 developing 121–4, 128–48, 141–8, 153–6 range 41–6, 49, 53–5, 114, 123, 170 in dispersal 189, 193, 205–6 rates 49, 55, 63, 138–42, 203 brood age 130–1, 141–2, 150–5 brood size 121–3, 132–6, 139–41, 152–5 parasites 63, 121–3, 134–5, 142 parental role 72, 80–3, 90, 138–40, 142, 145–8 time of day 40, 42, 118, 141, 185 weather 18, 26, 41–6, 82, 93, migration 141–2, 147, 151–2, 175, 192, 202 sites 40–6, 52–9, 89–106, 162–3, 173, 178, 182 techniques 15, 41–6, 82, 93, 141–2, 147, 151–2 fertile period 63, 69, 85, 90–1 fertilisers 204–6 Finland 17, 22, 24, 54, 119, 123 and productivity 151, 156, 187, 194–5, 198 Flanders 104, 199 fleas 139, 159 fledging 83, 93, 113, 131, 138 development 133, 144–6, 156, 168 fledglings 48, 56–7, 65–7, 73, 75, 83, development 93, 105, 121–2, 149–63, 193 flies 27–8, 32, 34, 36–45, 106, 175 flight 50, 64, 103, 133, 189 costs 18, 27, 29–30, 32–6, 41–5, 76–8, 186 foraging 15, 26–38, 105, 145–7, 154, 205

The Barn Swallow height 28–9, 45, 49, 55, 99–100, 129 migration 177, 185 manoeuvrability 15–17, 27–8, 30–6, 38–9, 47 migration 90, 177, 181, 183–6 mode 28–30, 36, 39, 69 speed 28–30, 33–4, 38, 49, 63, 84, 129, migrating 181, 188–6 flocks 78–9, 174, 185 Florida 22, 101, 175, 201 Flycatcher, Spotted 158, 211 food bolus 32, 39–40, 43–4, 139 foraging 15–16, 26, 36–46, 53–5, 170, 203–6 costs 25, 27–41, 76, 80–3, 127, 146–8, 188. for chicks 32, 34, 38–45, 95, 114, 119–23 and productivity 134, 140–8, 161 flight 28–32, 35, 92, 119, 154, 187, 191 techniques 28, 36, 39–46, 54, 103, 124, 184–5 France 151, 169, 173, 178–9, 183–4, 186, 195 gape 17, 51, 137, 143 colour of 137–8 geographical variation 24–5, 65 eggs 104, 106, 111, 113–4, 118–20, 122–6 mate choice 65, 72, 75–6, 89 moult and population 189–93, 198 productivity 150, 156, 173, 177 young 135–6, 144, 147, 150–6 Germany 38, 44, 46, 53–4, 85, 105, 115 migration 173, 180, 191, 194–5, population 199, 203–4, 206–7 productivity 151–2, 156, 167 Ghana 48, 173, 186, 191 Gibraltar 177, 184 Goshawk Grey 168, 210 Northern 168, 211 Red-chested 168, 211 Grackles, Boat-tailed 168, 210 Common 161, 168, 210 Great-tailed 168, 210

14639.qxd

24/1/06

3:54 pm

Page 251

Index grassland 16, 27, 41–6, 55–6, 99, 105–6, 132 and migration 176, 203, 205–6 grazing 41–3, 55–7, 99, 105–6, 132, 204–6 grit 37–8, 104 groups 17, 47–59, 60–3, 89–90, 93, 145, 194 anti-predator behaviour 41, 47, 55, 91, 95, 143–4 breeding success 54–9, 86–7, 113 foraging efficiency 47, 54–5, 142 nest site limitation 51–4, 57–9, 85 nest site quality 51–9, 207 predation 55 see also anti-predator and defence size 41, 47, 52–9, 85, 87, 93–7, 207 social benefits 47, 50, 53–9, 51, 95 traditional sites 56–9 Gulls, Californian 168, 210 habitats 16, 8, 41–6, 43–4, 59 breeding 98–100, 104–5 nests 112–13, 119, 132, 155–6 migration 176, 185, 192 and population 198, 204–8 haematocrit 34, 79, 117, 156 Haemoproteus prognei 159 hatching 89, 95, 143, 145, 163, 174 success 115–18, 121, 124–6, 128, 130 and productivity 150–6, 159–60 hatchling weight 116, 127, 130–3 hedgerows 41–5, 51, 53–4, 99, 204–6 Heron, Grey 51, 209 Hirundinidae 15–19, 29–32, 34–5, 46 migration 158–9, 168–70, 176, 185–6 social 51, 55, 66–7, 143 Hirundo aprica 18 rustica ambigua 20 erythrogaster 20–2, 115 insularis 22 gutteralis 20–3, 174 ‘kamschatica’ 20 mandschurica 20–2, 174 rustica 20–2, 24, 65, 115, 173–4 ‘saturata’ 20–2, 174 savugnii 20–1, 224, 174 transitiva 202, 174 tytleri 20–2, 174

251 Hobby African 168, 210 Eurasian 65, 168, 210 horses 27, 42, 46, 53, 104, 189, 204, 206 huddling behaviour 48, 51, 140, 170 humans 46, 144, 161, 169, 204 Humingbirds 170 hunting 16, 27, 34, 39–46, 171, 185 hybridisation 20, 22–3 hygiene on farms 99, 204, 206–7 hypothermia 170 Iceland 198 immune response 17, 32, 73, 75–6, 79, 116–17, in development 134–6, 147, 155, 160–2, 167 immunocompetence 82, 117–18, 154 adults 122–3, 157, 160, 163 chicks 75, 121–2, 134–7, 157–61, 154–6 immunoglobulin 117 incubation 65–6, 69–70, 19, 121–8, 156, 164–6 bouts 95, 124–5 duration 64, 100, 121–2, 123–6, 152 male and female roles, 35, 52, 64–6, 76, 106, 122–8 and fledglings 144, 147, 191 period of 23–6, 128 independence, age of 145–6, 193–6 India 19, 20, 49, 174–5, 184 Infanticide 56, 93–6, 158, 161, 202 infidelity see extra-pair copulations; extra-pair paternity insects 15, 25–7, 27–30, 54–6, 176, 204–8 abundance of 34, 37–46, 55, 100, 105 and breeding 112–22, 127, 132–7, 175–8, 185 in adult diet 36–9, 46, 185, 198, 202–8 in chick diet 38–45, 78, 130–3, 139–42 effect of weather 28, 42–6, 99, 141–2, 149–56, on migration 170, 188–2 Iran 176, 184, 192–3 Iraq 118, 184, 191–2 Ireland 169, 173, 175–6, 183–6, 194–5, 198 Italy 16–17, 22–4, 26, 36, 41 breeding 51, 58, 79, 87–9

14639.qxd

24/1/06

3:54 pm

Page 252

252 eggs 114, 116, 120, 136, 138 migration 175, 178–9, 183–4, 186–7 nest, 101, 105, 194 population 198, 202 song 60–3, 96, 101, 106 survival 150–2, 154–9, 167 Jaeger, Parasitic 168 Japan 20, 54, 101, 103, 106, 158, 206 migration 174–8, 184 Kazakhstan 167, 174, 200, 203, 207–8 Kestrel American 168, 210 Grey 168, 210 Kite, Yellow-billed 168, 211 Laos 169, 175 laying see egg-laying lice, feather 38, 42, 63, 73, 79, 159 Lime 42, 209 livestock 41–2, 53, 57–8, 101, 104–6, 114, 204 longevity 25, 70–2, 74, 111, 155, 167–8 louse flies 36, 63, 73, 134, 142, 159, 161, lutein 116–17 lysozyme 117–18, 135, 147, 156 Magpie, Common 161, 210 males, unmated 48–50, 56, 64, 69, 84–5, 92–6 survival 155, 166 maize 41, 209 Martin 15–16, 18 African River 17–18, 210 Banded 18, 210 Brazza’s 18, 210 Collared Sand 16, 18, 22, 32, 34, 48–9, 210 Mascarene 18, 211 Northern House 15, 22–3, 32–4, 48, 51, 99, 157–8, 211 Purple 16, 211 White-eyed River 17–18, 211 mate choice 17, 32, 35, 95 females 63–4, 68–76, 77–86, 114, 195 males 69–70, 72–7, 82–3, 84, 195–6 mate-guarding 56, 64, 79, 85–6, 90–7, 144

The Barn Swallow mayflies 36, 38, 43–6 melanin 23, 80 Merlin 168, 211 migration 26, 28–9, 35–8, 163–4, 168–9, 208 routes 113–14, 176–8, 183, 203, 206 speed 28, 181, 183–6 timing in autumn 38, 175–8, 183–8 timing in spring 58, 69, 75, 88, 113–14, 128 migrating 175–83, 195, and survival 152, 167, 170–1 weather 17, 26, 169–71, 181, 184–6, and population 203, 206 mites, tropical fowl 56, 63, 73–5, 77, 110–11 and development 122, 120, 134–6, 143, 159–61 mixed farming 42–3, 46, 53–4, 58 and population 185–202, 204–7 and survival 152, 154, 156, 159–62, 156 mobbing see defence of offspring mortality 26, 95, 97, 149, 161, 166–71, 202–5 chicks 93, 121, 130, 143, 150, 156–62, 164–8, early arrival 73–5, 92–3, 169–70, 182, 202 eggs 56, 143, 158–61, 202 females 117, 128, 155–61, 202 fledglings 56, 82–3, 117, 162–3, 168–71, 201–2 males 75, 155, 163–9, 182 migration 171, 169–70, 182, 201–8 winter 167–8, 170, 201–8 moths 37–8, 40, 43, 46, 159 moult 38, 174, 189–93, 208 effects of weather 26, 36, 77, 170–1, 178 juvenile 25, 192–3 speed 171–1, 189, 190–3 timing 38, 178, 182–3, 187–93, 208 natal philopatry see dispersal, natal Nebraska 17, 93, 166–7 nest-building 16, 51, 69, 81, 95, 107–11 population 193, 203–5

14639.qxd

24/1/06

3:54 pm

Page 253

Index nest-guarding 52, 56, 63, 69, 75, 81, breeding 85–89, 90–7, 144 egg-dumping 56–66 , 96 infanticide 53, 93–6, 158, 161, 202 nestling period 129–44 nests 16–18, 67, 158–61, 178, 186, 201–8 artificial 99–100, 102, 104 competitors 85, 92, 95, 157–8, 185, 202, 207 desertion 115, 121, 128, 138–9, 156–7, 161–2 failure 97, 103, 121, 149–50, 161, 195–6, 198, lining 51, 103, 107–9, 125, 145, 168 moving 102–3 predators 51–3, 57, 110, 163, 207 re-use 48, 52, 57–9, 69, 103, 108–11 productivity 150, 152, 162, 170, 194–8, 207 sites 16, 18, 22–3, 41, 59–60, 99–102, and migration 183, 193–4, 206–8 on artefacts 16, 18, 22–3, 51–3, 66–9, 123 natural 18, 48, 51–3, 98, 103–4, 106–7 and environment 158, 199, 206 size 51–3, 57–8, 107–9, 120 spacing 16, 41, 51–3, 56–7, 67 breeding 87–9, 93–4, 103, 110–11, 123, 206 structure 18, 52, 107–9, 157–8, 161, 203 Netherlands 102, 104–5, 173 New York State 17, 56, 76, 87, 97 productivity 151, 156, 159, 194–5, 181 Nigeria, 169, 173, 169 Normalised Difference Vegetation Index (NDVI) 171, 178–9, 181, 202 North Africa 16–19, 35, 99, 203 migration 175, 177, 184–5, 188, 191–2, 194, 203 North America 16–25, 35–6, 41, 51–3, 56–9 breeding 96, 99–101, 103–4, 107 courrtship 65, 68, 70–6, 82–3, 85–7, 89 eggs and chicks 114–15, 123–4, 134, 144, 161 fledglings 151–8, 161–2, 167

253 migration 168–70, 175, 177, 181, 184, 191–2, 200–7 North Atlantic Oscillation (NAO) 114, 119–20, 135, 153–4, 156 and dispersal 181, 186, 203 Oak 42, 209 oilseed rape 41, 205, 209 Ontario 20, 70, 76, 87 101, 201 orientation 183–5 Orkney 101, 198, 204 Owl Barn 168, 206, 210 Tawny 161, 168, 211 pair bond duration 56, 81–3, 87, 97 pair formation 69, 76, 84–90, 95–7 Pakistan 20, 173–5, 184 parasites 50, 55–6, 77, 87, 87, 95–6 and development 125, 137, 142, 158–61 blow fly larvae 28, 56, 134, 145, 150–5, 158, 209 effects of 63, 73, 86, 89 in nests 110, 117, 120–1, 125, 134–6, 142 parental care 145, 150–5, 159–61, 185, 192 feather lice 36, 63, 73, 77, 79–80 survival 154, 157, 159–63, 209 fleas 159, 209 louse flies 63, 73, 134, 142, 159, 161, 209 mites, tropical fowl 56, 73–4, 77, 110–11, 122 chicks 134–6, 143, 145, and productivity 151–2, 154, 159, 162, 209 resistance to 32, 73–5, 81, 117, 121–3 chicks 130, 134–6, 150–2, 160–1, parental care, role of sexes 72, 80–3, 89–92 development 103–4, 108, 123–6, 136, 138–44, 153–4 pasture 41–6, 53–5, 105–6, 176, 204–6 parental characteristics 153–5 paternity 56–7, 80–90, 142, 144, see also extra-pair pesticides 106, 157, 169, 204–6

14639.qxd

24/1/06

3:54 pm

Page 254

254 Phoebe Eastern 158, 210 Say’s 158, 211 pigs 46, 53, 104–5 plumage 16–18, 130, 133–4, 157 coloration 15–18, 20–5, 66, 68–72, 76, 80–3 and productivity 133, 190, 192 dimorphism 23–5, 80 hybrids 22–3 juvenile 25, 66–7, 133, 146, 192–3 variation 20–4 Poland 37, 54, 101, 104, 181, 200 pollution 97, 107, 157, 204–5 polygyny 92–3, 97 population 17–18, 176, 198–208 nest site availability 51–9, 85, 194–6, 204–8 declines 53, 85, 149, 157–8, 166, 169, 197–202, 204–8 density 53–9, 94, 120, 166, 168, 198, 201 trends 53, 96, 101, 198–200, 202–5 effects of weather 75, 168–71, 186, 201–3 Poorwills 170 predators 41, 48–9, 51, 65, 77, 189, 200 on nests 55, 57, 91, 95, 102–4, 110, 143–4, and population 195, 207 productivity 143–4, 149, 158, 161–2, 167–8, 188 preening 16, 47, 50–2, 69, 104, 134, 143 productivity 16, 79, 82–3, 121–3, 125, 150–6 promiscuity 85–90 see also extra-pair and paternity provisioning rates see feeding rates races 18–19, 20–5, 65, 113, 115, 178 Racoon 161, 211 Rat 161, 169, 211 recognition 66 of chicks by parents 47–8, 66–7, 142, 145–6, of eggs by parents 66, 96 recruitment 58, 83, 85, 88, 138, 149–71 productivity 155–6, 159–63, 193, 197, 201–3, 208

The Barn Swallow Redstart, Black 51, 102, 158, 210 return rates 57–9, 69, 95, 103, 153–5, 162–3, 166 and migration 176, 193–7, 207 Robin American 102, 210 European, 102, 158, 210 roost 48–50, 52, 170–4, 185, 187 composition 48–9, 192 population 168–76, 192–4, 206 reedbeds 47–9, 169–70, 184–5, 188, 206 size 48–9 towns 16, 48–9, 185, 200 trees 48–9, 145 Royal Society for the Protection of Birds (RSPB) 169 Russia 20–2, 24, 26, 37, 46, 53–4, 200 breeding 31, 100–2, 119, 123 migration 170, 174–5, 177, 181, 186, 206 Sahara 26, 171, 184–8, 186–90, 203 Sahel 171, 178, 181, 184 savannah 16, 42, 203 Saw-wing, Square-tailed 16, 211 Scandinavia 19–20, 54, 56, 99.198 migration 173, 177–8, 181, 184 Scotland 16, 24–5, 28, 32–45 breeding 51, 54, 58, 79, 82–3 building 93, 96–7, 100–5, 108 eggs 115–20, 122, 126–7 juveniles 130, 132–3, 140–6, 150–6, 161–3 migration 176–82, 187, 194–5, 198, 202 survival 166–7 second broods 52, 71, 90, 96, 109–11, 113 breeding 109–11, 113, 117–29, 132, 135–6, 144–5 feeding rates 28, 39, 80–1, 141, 208 percentage of 71–2, 78, 110, 125, 208 and productivity 150–2, 153–5, 159–62, 202 senescence 76, 153–4, 166–8 set-aside 41 sex allocation 142–3 sex identification 23–6, 32–3, 36, 60, 64–7, sex ratio 90, 93–7, 143–4,

14639.qxd

24/1/06

3:54 pm

Page 255

Index sexual dimorphism 20, 23–6, 32–4, 36, 64–7, 82 sheep105–6, 205, 208 shelterbelts 41–3, 45, 106, 185 Siberia 19–20, 38, 123–4, 173, 184, 204 song 16, 51, 59–67, 69–70, 94 duration 41, 60–4, 108 effects of parasites 63, 76 quality 60–4, 70, 76 rate of singing 60–4, 76, 88–91 subsong 60 syllable repertoire 60–6 South America 18–19, 22, 174, 177, 184–5 Spain 16–17, 22, 24–6, 34, 36, 39, 42, 63, breeding 69, 78–80, 82–90, 92, 113 chicks 134–6, 144–5, 141, 147 fledglings 151–2, 156–7, 159 migration 173, 175, 178–9, 184, 189–93, 198 song 60, 63 Sparrow European Tree 158, 210 House 46, 51, 149, 158, 161, 200, 210 Sparrowhawk, Eurasian 41, 65, 75, 78, 144, 167–8, 210 Squirrel, Red 161, 211 Starling, European 49, 66, 158, 178, 210 starvation 55, 90, 130, 132, 139, 156, 170 subspecies see races sunbathing 47, 50, 100 survival 16, 25–6, 197, 203 survival rates 32, 55, 78, 83, 90, 121, 123 productivity 149, 155, 162–71, 182, 198, 203 adults 74–5, 78–83, 149, 164–71 first-years 26, 135, 153, 162–5, 168–71, 193 fledglings 73, 86, 149, 162–3, 168–71, 152 Swallow Angolan 19 Black-collared 16, 210 Black-and-Rufus 19 Blue 19 Cave 22–3, 158, 210 Cliff 16, 18, 22–3, 51–2, 54–5, 66–7, 102, 158, 210 Ethiopian 16, 18–19, 22, 210

255 Grey-rumped 17–18, 210 Mangrove 16, 211 Pacific 18, 19, 211 Pied-winged 19 Pearl-breasted 19 Red-chested 18–19, 22 Red-rumped 22, 35, 157–8, 211 Tree 16, 18, 66, 157–8, 211 Welcome 18–19, 22, 211 White-backed 18, 211 White-banded 16, 211 White-tailed 16, 19, 211 White-thighed 15, 211 White-throated Blue 18–19, 211 Wire-tailed 19 sward height 105, 132 Swift Common 32, 210 Horus 210 House 210 Little 211 White-rumped 211 Switzerland 35, 41–5, 54, 56, 99–100, productivity 147, 151, migration 176–7, 191, 199, 203 tail 16, 63–4, 80–3, 191 evolution of 17, 32–6, 72–4, 76 length 16, 23–5, 30–6, 154–5 fledglings 150, 154–5 mating 56, 63–4, 69, 70–83, 86, 88, 92–3 nesting 108, 114, 123, 133–6, 138, 143 productivity 150, 163, 182, 188, 202 muscles 32, 35, 163, 170 outer feathers 17, 24–5, 30–5, 45, 70, 79–80 migration 133–6, 171, 190–3 spots 16–17, 23–5, 70–2, 76, 80 symmetry 24–6, 33–6, 71–3, 76–7, 80–1, 89 migration 154, 192 use in flight 30–6, 38, 71, 77, 171 tarsus 17, 23–5, 132–4, 139, 155–6, 164 taxonomy 15–23 temperature cold 48, 51, 75, 84, 100, 126–71, 203

14639.qxd

24/1/06

3:54 pm

Page 256

256 egg 105, 107, 110–27, 148 heat 28, 34, 39, 50–1, 121, 141, 162, 186 regulation 104–5, 107, 121, 124–8, 136, 207 warmth 119–20, 141, 103, 182 see also body temperature; climate change; weather termites 17, 37–8, 46–7, 81, 91, 171 territory size 16, 52, 69, 90–3, 102, 182 testes size 88–92 testosterone 61–2, 79, 92, 139–40 thermoregulation see temperature regulation, 139–40 Thailand 169, 174–5 Thrush, Song 102, 131, 170, 211 timing of breeding 56, 58, 69, 82–9, 93, 96–7, in nest 100, 108, 112, 118–19, 141 of migration 75, 146, 175–85 productivity 150–2, 156, 161–3, 202–3, 208 Tits 17 Blue 72, 210 torpor 170, 172 tundra 99–100 Ukraine 22–3, 198 unpaired males see males, unmated vagrants 19 warblers 17 wasps 36–7, 40, 102, 159 weather, effect of 48–9, 147, 205–8 on breeding success 55, 113, 122–3, 140, 153 on chick growth 50, 130–6, 141–2 on egg-laying 42, 82, 109, 113–23, 126–8, 153–4 on foraging 41–6, 49, 54, 108, 113–23 for young 141–2, 146, 153 on incubation 121–8, 195 on insects 28, 36, 42–5, 113–23, 128 for juveniles 132, 141–2, 155–6, 169–70 on migration 26, 168–80, 169–80

The Barn Swallow on moult 170 on productivity 58, 82–3, 115–23, 150–5 on survival 26, 75, 92–3, 122 on timing of breeding 48, 82, 104–6, 108–9, 113–115, 149–50 temperatures 28, 34, 39–46, 50, 75 and chicks 115–25, 132, 141, 147–9, 153, 156 migration 169–70, 178–81, 185–6, 192 nests 100, 106, 108, 147 rainfall 42, 75, 77, 75, 103 , and migration 170–1, 178, 189, 192, 203 and nests 111, 122, 131, 156 wind 41–2, 45, 110, 130, 171, 181–9, 192 Weasel 161, 211 weights 15, 23, 30–1, 163–8 chicks 55, 118, 130–6, 142–3, 152, 162–3, during breeding 82–3, 92, 124–8, 146–7, 162–3 during migration 187–90, 193 over winter 170–1, 187 White-eyes 17 wind speed 41, 45 wind tunnels 28–31 wings 16–17, 29–32, 40, developing 135, 140, 145, 154, 156, 190–3 beat rate 28–9, 31 length 17, 20, 23–6, 29, 31 development 131–3, 155, 165 loading 30, 33, 131–2 wingspan 29, 124, 133, 155 winter quarters 20–2, 26, 36–8, 48–9, 69, 75–7 migration 173–6 population 197, 202–8 survival 163–71, 189–93 woodland 41, 52–4, 99–101, 176 as shelter 180–1, 186, 189–93, 197, 202–8 Wren House 168, 210 Winter 158, 211