Landscape Ecology

, Volume 27, Issue 10, pp 1395–1405 | Cite as

Agricultural intensification exacerbates female-biased primary brood sex-ratio in tree swallows

  • Renaud Baeta
  • Marc Bélisle
  • Dany GarantEmail author
Research Article


Impacts of agriculture practices are documented at every ecosystem level from landscape structure to biodiversity. Birds are especially affected by agricultural modifications as shown by the decline of farmland species in Europe and North America. Few studies have assessed the effects of such modifications on individual characteristics directly influencing population dynamics. Several bird studies showed that sex-ratio may be adaptive and that mother condition affects the production of sons and daughters. However, little is known about the connections between environmental and individual characteristics on sex allocation. Here we quantified the variation in primary sex-ratio in tree swallows (Tachycineta bicolor) nesting in contrasted environments associated with agricultural intensification in southern Québec, Canada. We found that intensive agricultural practices affected female sex-ratio allocation in this area, resulting in more biased sex-ratio towards daughters throughout most of the hatching period. Yet, this bias towards daughters was reduced as the season progressed in the most intensively cultivated areas, suggesting that tree swallows have problems foreseeing the difficult growth and postfledging conditions that their nestlings will experience in such environments. Our results thereby support the hypothesis that intensive agricultural areas act as an ecological trap in our study system. We also found that effects of agricultural intensification on sex allocation differed among years and affected the relationships between sex-ratio allocation and hatching date. Our results suggest that agricultural intensification modifies female sex allocation in tree swallows, but the importance of the effects might vary among years and depend on timing of breeding.


Agriculture Environmental change Landscape structure Phenology Primary sex-ratio Tachycineta bicolor 



We thank all the research assistants who helped collecting data in the field over the years and the 40 farm owners who allowed us to use their land for our research. We acknowledge M. Lieutenant-Gosselin, C. Gayet and A. Lessard for their help with laboratory work. We thank D. Bender and two anonymous reviewers as well as G. Gauthier, M. Festa-Bianchet and F. Pelletier for comments on a previous draft of the manuscript. This work was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants (DG and MB), by the Canada Research Chair in Spatial and Landscape Ecology (MB), as well as by the Canadian Foundation for Innovation (DG and MB).


  1. Baeta R, Bélisle M, Garant D (2012) The importance of maternal investment in studies of sex-ratio adjustment: a case study using tree swallows. Biol Lett 8:401–404PubMedCrossRefGoogle Scholar
  2. Battin J (2004) When good animals love bad habitats: ecological traps and the conservation of animal populations. Conserv Biol 18:1482–1491CrossRefGoogle Scholar
  3. Bélanger L, Grenier M (2002) Agriculture intensification and forest fragmentation in the St. Lawrence valley, Québec, Canada. Landscape Ecol 17:495–507CrossRefGoogle Scholar
  4. Benton TG, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687CrossRefGoogle Scholar
  5. Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188CrossRefGoogle Scholar
  6. Bishop CAB, Collins P, Mineau P, Burgess NM, Read WF, Risley C (2000) Reproduction of cavity-nesting birds in pesticide-sprayed apple orchards in southern Ontario, Canada, 1988–1994. Environ Toxicol Chem 19:588–599Google Scholar
  7. Bradbury RB, Kyrkos A, Morris AJ, Clark SC, Perkins AJ, Wilson JD (2000) Habitat association and breeding success of yellowhammers on lowland farmland. J Appl Ecol 37:789–805CrossRefGoogle Scholar
  8. Brickle NW, Harper DGC, Aebischer NJ, Cockayne SH (2000) Effects of agricultural intensification on the breeding success of corn buntings Miliaria calandra. J Appl Ecol 37:742–755CrossRefGoogle Scholar
  9. Britschgi A, Spaar R, Arlettaz R (2006) Impact of grassland farming intensification on the breeding ecology of an indicator insectivorous passerine, the Whinchat Saxicola rubetra: lessons for overall Alpine meadowland management. Biol Conserv 130:193–205CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002). Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  11. Canadian Wildlife Service (2004) Occupation du sol à partir des images classifiées Landsat-7, Sud du Québec, 1999–2003. Environnement Canada, région du Québec, Québec, CanadaGoogle Scholar
  12. Cassey P, Ewen JG, Møller AP (2006) Revised evidence for facultative sex-ratio adjustment in birds: a correction. Proc R Soc B 273:3129–3130PubMedCrossRefGoogle Scholar
  13. Chamberlain DE, Fuller RJ, Bunce RGM, Duckworth JC, Shrubb M (2000) Changes in abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. J Appl Ecol 37:771–788CrossRefGoogle Scholar
  14. Charnov EL (1982) The theory of sex allocation. Princeton University Press, New JerseyGoogle Scholar
  15. Collins BT, Downes CM (2009) Canadian Bird Trends Web site Version 2.3. Canadian Wildlife Service, Environment Canada, Gatineau, Quebec, K1A 0H3Google Scholar
  16. Dawson RD (2008) Timing of breeding and environmental factors as determinants of reproductive performance of tree swallows. Can J Zool 86:843–850CrossRefGoogle Scholar
  17. Delmore KE, Kleven O, Laskemoen T, Crowe SA, Liffield TJ, Robertson RJ (2008) Sex allocation and parental quality in tree swallows. Behav Ecol 19:1243–1249CrossRefGoogle Scholar
  18. Donald RF, Green RE, Health MF (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc R Soc B 268:25–29CrossRefGoogle Scholar
  19. Dunn PO, Whittingham LA (2005) Radio-tracking of female tree swallows prior to egg-laying. J Field Ornithol 76:259–263Google Scholar
  20. Dunn PO, Winkler DW, Whittingham LA, Hannon SJ, Robertson RJ (2011) A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92:450–461PubMedCrossRefGoogle Scholar
  21. ESRI (2005) Patch analyst 2.0a patch for French language. ESRI. Redlands. CaliforniaGoogle Scholar
  22. Evans AD, Smith KW (1994) Habitat selection of Cirl Bunting Emberiza cirlus wintering in Britain. Bird Study 41:81–87CrossRefGoogle Scholar
  23. Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107CrossRefGoogle Scholar
  24. Fuller RJ, Gregory RD, Gibbons DW, Marchant JH, Wilson JD, Baillie SR, Carter N (1995) Population declines and range contractions among lowland farmland birds in Britain. Conserv Biol 9:1425–1441CrossRefGoogle Scholar
  25. Gates JE, Gysel LW (1978) Avian nest dispersion and fledging success in field–forest ecotones. Ecology 59:871–883CrossRefGoogle Scholar
  26. Gebhardt-Henrich SG, van Noordwijk AJ (1991) Nestling growth in the Great Tit I. Heritability estimates under different environmental conditions. J Evol Biol 3:341–362CrossRefGoogle Scholar
  27. Ghilain A, Belisle M (2008) Breeding success of tree swallows along a gradient of agricultural intensification. Ecol Appl 18:1140–1154PubMedCrossRefGoogle Scholar
  28. Green RE, Stowe TJ (1993) The decline of the corncrake in Britain and Ireland in relation to habitat change. J Appl Ecol 30:689–695CrossRefGoogle Scholar
  29. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  30. Heinsohn R, Legge S, Barry S (1997) Extreme bias in sex allocation in Eclectus parrots. Proc R Soc B 264:1325–1329CrossRefGoogle Scholar
  31. Hole DG, Whittingham MJ, Bradbury RB, Anderson GQA, Lee PLM, Wilson JD, Krebs JR (2002) Widespread local house-sparrow extinctions-agricultural intensification is blamed for the plummeting populations of these birds. Nature 418:931–932PubMedCrossRefGoogle Scholar
  32. Howe HF (1977) Sex-ratio adjustment in the common grackle. Science 198:744–746CrossRefGoogle Scholar
  33. Hussell D (1983) Age and plumage color in female tree swallows. J Field Ornithol 54:312–318Google Scholar
  34. Jobin B, Grenier M, Laporte P (2005) Using satellite imagery to assess breeding habitat availability of the endangered loggerhead shrike in Quebec. Biodivers Conserv 14:81–95CrossRefGoogle Scholar
  35. Johnson LS, Wimmers BG, Johnson RC, Milkie EC, Molinaro RL, Gallagher BS, Masters BS (2005) Sex manipulation within broods of house wrens? A second look. Anim Behav 70:1323–1329CrossRefGoogle Scholar
  36. Kempenaers B, Everding S, Bishop C, Boag P, Robertson RJ (2001) Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor). Behav Ecol Sociobiol 49:251–259CrossRefGoogle Scholar
  37. Komdeur J, Daan S, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex-ratio of the Seychelles warbler’s eggs. Nature 385:522–525CrossRefGoogle Scholar
  38. Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM (1999) The second silent spring? Nature 400:611–612CrossRefGoogle Scholar
  39. Lamoureux S (2010) Impact de l’intensification agricole sur l’effort parental, la croissance et la survie des oisillons chez l’Hirondelle bicolore (Tachycineta bicolor). M. Sc. Thesis, Université de Sherbrooke, Sherbrooke, Québec, CanadaGoogle Scholar
  40. Lawton JH, May RM (1995) Extinction rates. Oxford University Press, OxfordGoogle Scholar
  41. Lenz TL, Jacob A, Wedekind C (2007) Manipulating sex-ratio to increase population growth: the example of the Lesser Kestrel. Anim Conserv 10:36–244Google Scholar
  42. Lessells CM, Mateman AC, Visser J (1996) Great tit hatching sex-ratios. J Avian Biol 27:135–142CrossRefGoogle Scholar
  43. Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 25:504–509CrossRefGoogle Scholar
  44. McCarty JP, Winkler DW (1999) Foraging ecology and diet selectivity of tree swallows feeding nestlings. Condor 101:246–254CrossRefGoogle Scholar
  45. Meyer WB, Turner BL (1992) Human population growth and global land-use/cover change. Annu Rev Ecol Syst 23:39–61CrossRefGoogle Scholar
  46. Müller M, Spaar R, Schifferli L, Jenni L (2005) Effects of changes in farming of subalpine meadows on a grassland bird, the whinchat (Saxicola rubetra). J Ornithol 146:14–23CrossRefGoogle Scholar
  47. Nager RG, Monaghan P, Griffiths R, Houston DC, Dawson R (1999) Experimental demonstration that offspring sex-ratio varies with maternal condition. PNAS 96:570–573PubMedCrossRefGoogle Scholar
  48. Nebel S, Mills A, McCracken JD, Taylor PD (2010) Declines of aerial insectivores in North America follow a geographic gradient. Avian Cons Ecol 5:1Google Scholar
  49. North American Bird Conservation Initiative, U.S. Committee (2009) The State of the Birds. United States of America, 2009. U.S. Department of Interior: Washington, DC, pp 1–36Google Scholar
  50. Peach WJ, Siriwardena GM, Gregory RD (1999) Long-term changes in over-winter survival rates explain the decline of reed buntings Emberiza schoeniclus in Britain. J Appl Ecol 36:798–811CrossRefGoogle Scholar
  51. PECBMS (2009) The State of Europe’s Common Birds. CSO/RSPB, Prague, pp 1–28Google Scholar
  52. Pimentel D, Stachow U, Takacs DA, Brubaker HW, Dumas AR, Meaney JJ, O’Neil JAS, Onsi DE, Corzilius DB (1992) Conserving biological diversity in agricultural/forestry systems. Bioscience 42:354–362CrossRefGoogle Scholar
  53. Porlier M, Bélisle M, Garant D (2009) Non-random distribution of individual genetic diversity along an environmental gradient. Philos Trans R Soc B 364:1543–1554CrossRefGoogle Scholar
  54. Potts GR (1991) The environmental and ecological importance of cereal fields. In: Firbrank LG, Carter N, Darbyshire JF, Potts RR (eds) The ecology of temperate cereal fields. Blackwell Scientific, Oxford, pp 3–21Google Scholar
  55. Potts GR (1997) Cereal farming, pesticides and grey partridges. In: Pain J, Pienkowski MW (eds) Farming and birds in Europe. Academic Press, London, pp 150–177Google Scholar
  56. Prior GL, Evans DM, Redpath S, Thirgood SJ, Monaghan P (2011) Birds bias offspring sex-ratio in response to livestock grazing. Biol Lett 7:958–960PubMedCrossRefGoogle Scholar
  57. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267CrossRefGoogle Scholar
  58. Rioux-Paquette S, Garant D, Pelletier F, Bélisle M (2012) Seasonal patterns in tree swallow prey (Diptera) abundance are affected by agricultural intensification. Ecol Appl. doi: 10.1890/12-0068.1
  59. Robertson RJ, Stutchbury BJ, Cohen RR (1992) Tree swallow (Tachycineta bicolor). In: Poole A, Stettenheim P, Gill FB (eds) The birds of North America. Academy of Natural Sciences, Washington, pp 1–28Google Scholar
  60. Robertson BC, Elliott GP, Eason DK, Clout MN, Gemmell NJ (2006) Sex allocation theory aids species conservation. Biol Lett 22:229–231CrossRefGoogle Scholar
  61. Robinson RA, Sutherland WJ (2002) Post-war changes in arable farming and biodiversity in Great Britain. J Appl Ecol 39:157–176CrossRefGoogle Scholar
  62. Roschewitz I, Gabriel D, Tscharntke T, Thies C (2005) The effects of landscape complexity on arable weed species diversity in organic and conventional farming. J Appl Ecol 42:873–882CrossRefGoogle Scholar
  63. Sheldon BC (1998) Recent review of avian sex-ratio. Heredity 80:397–402CrossRefGoogle Scholar
  64. Shutler D, Hussell DJT, Norris DR, Winkler DW, Robertson RJ, Bonier F, Rendell WB, Bélisle M, Clark RG, Dawson RD, Wheelwright NT, Lombardo MP, Thorpe PA, Truan MA, Walsh R, Leonard ML, Horn AG, Vleck CM, Vleck D, Rose AP, Whittingham LA, Dunn PO, Hobson KA, Stanback MT (2012) Spatiotemporal patterns in nest box occupancy by tree swallows across North America. Avian Cons Ecol 7:3Google Scholar
  65. Smits JEG, Bortolotti GR, Sebastian M, Ciborowski JJH (2005) Spatial, temporal, and dietary determinants of organic contaminants in nestling tree swallows in Point Pelee National Park, Ontario, Canada. Environ Toxicol Chem 24:3159–3165PubMedCrossRefGoogle Scholar
  66. Sotherton NW (1998) Land use changes and the decline of farmland wildlife: an appraisal of the set-aside approach. Biol Conserv 83:259–268CrossRefGoogle Scholar
  67. Stapleton MK, Robertson RJ (2006) Female tree swallow home-range movements during their fertile period as revealed by radio-tracking. Wilson J Ornithol 118:502–507CrossRefGoogle Scholar
  68. Stearns SC (1976) Life history tactics: a review of ideas. Q Rev Biol 51:3–47PubMedCrossRefGoogle Scholar
  69. Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185–190CrossRefGoogle Scholar
  70. Swift MJ, Anderson JM (1993) Biodiversity and ecosystem function in agroecosystems. In: Schultze E, Moone HA (eds) Biodiversity and ecosystem function. Springer, New York, pp 57–83Google Scholar
  71. R Development Core Team (2009) R: a language and environment for statistical computing. R Development Core Team, ViennaGoogle Scholar
  72. Thrall PH, Bever JD, Burdon JJ (2010) Evolutionary change in agriculture: the past, present and future. Evol Appl 3:405–408CrossRefGoogle Scholar
  73. Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284PubMedCrossRefGoogle Scholar
  74. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex-ratio of offspring. Science 179:90–92PubMedCrossRefGoogle Scholar
  75. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity: ecosystem service management. Ecol Lett 8:857–874CrossRefGoogle Scholar
  76. Velando A, Graves J, Ortega-Ruano JE (2002) Sex-ratio in relation to timing of breeding, and laying sequence in a dimorphic seabird. Ibis 144:9–16CrossRefGoogle Scholar
  77. Verhulst S, Nilsson JA (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc B 363:399–410CrossRefGoogle Scholar
  78. Vickery JA, Evans AD, Grice P, Brand-Hardy R, Aebischer NA (2004) Ecology and conservation of lowland farmland birds II: the road to recovery. Ibis 146(Suppl 2):1–258Google Scholar
  79. Wedekind C (2012) Managing population sex ratios in conservation practice: how and why? In: Povilitis T (ed) Topics in conservation biology. ISBN: 978-953-51-0540-4. InTech. doi: 10.5772/37601
  80. West SA, Sheldon BC (2002) Constraints in the evolution of sex-ratio adjustment. Science 295:1685–1688PubMedCrossRefGoogle Scholar
  81. Whittingham LA, Dunn PO (2000) Offspring sex-ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129PubMedCrossRefGoogle Scholar
  82. Wilby A, Thomas MB (2002) Natural enemy diversity and pest control: pattern of pest emergence with agricultural intensification. Ecol Lett 5:353–360CrossRefGoogle Scholar
  83. Wilson K, Hardy ICW (2002) Statistical analysis of sex-ratios: an introduction. In: Hardy ICW (ed) Sex-ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 48–92CrossRefGoogle Scholar
  84. Wilson JD, Evans AD, Grice PV (2009) Bird conservation and agriculture. Cambridge University Press, CambridgeGoogle Scholar
  85. Winkler DW, Allen PE (1996) The seasonal decline in tree swallow clutch size: physiological constraint or strategic adjustment. Ecology 77:922–932CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Département de Biologie, Faculté des SciencesUniversité de SherbrookeSherbrookeCanada

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