Spatial heterogeneity and structure of bird populations: a case example with the eagle owl

Abstract

If individuals of the same population inhabit territories different in landscape structure and composition, experiencing habitat-specific demographic rates, then the landscape features become major determinants of the overall population characteristics. Few studies have tested how habitat-specific demography interacts with landscape heterogeneity to affect populations of territorial species. Here we report a 29-year study of an eagle owl (Bubo bubo) population in southern France. The aim of this study was to analyse how habitat heterogeneity could affect density and breeding performance. Mean productivity for the overall sample was 1.69±0.76 fledglings per breeding pair and, after controlling for year effect, significant differences between territories were detected for productivity. A positive correlation was found between the percentage of pairs producing 50% of the annual fledged young (an index of the distribution of fecundity among nesting territories) and the mean reproductive outputs, that is the heterogeneous structure of the population determined that most/all pairs contributed to the annual production of young during good years, but the opposite during poor years (i.e. fewer pairs produced the majority of fledglings). Mean reproductive output was positively affected by percentage of open country and diet richness. Although other factors different to territory quality could affect demography parameters (e.g. quality of breeders), our results clearly showed a significant correlation between landscape features and population productivity.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Andrén H (1990) Despotic distribution, unequal reproductive success, and population regulation in the Jay Garrulus glandarius L. Ecology 71:1796–1803

    Google Scholar 

  2. Aron S, Keller L, Passera L (2001) Role of resource availability on sex, caste and reproductive allocation ratios in the Argentine ant Linepithema humile. J Anim Ecol 70:831–839

    Article  Google Scholar 

  3. Berg Å (1997) Diversity and abundance of birds in relation to forest fragmentation, habitat quality and heterogeneity. Bird Study 44:355–366

    Google Scholar 

  4. Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford

  5. Blondel J, Badan O (1976) La biologie du Hibou grand-duc en Provence. Nos Oiseaux 33:189–219

    Google Scholar 

  6. Blondel J, Perret P, Maistre M, Dias PC (1991) Do harlequin Mediterranean environments function as source sink for Blue Tits (Parus caeruleus)? Land Ecol 6:213–219

    Google Scholar 

  7. Blondel J, Dias PC, Maistre M, Perret P (1993) Habitat heterogeneity and life-history variation of Mediterranean Blue Tits (Parus caeruleus). Auk 110:511–520

    Google Scholar 

  8. Boecklen WJ (1986) Effects of habitat heterogeneity on the species-area relationship of forest birds. J Biogeogr 13:59–68

    Google Scholar 

  9. Bollmann K, Reyer HU, Brodmann PA (1997) Territory quality and reproductive success: can water pipits Anthus spinoletta assess the relationship reliably? Ardea 85:83–98

    Google Scholar 

  10. Both C (1998) Density dependence of clutch size: habitat heterogeneity or individual adjustment? J Anim Ecol 67:659–666

    Article  Google Scholar 

  11. Brönmark C (1985) Freshwater snail diversity: effects of pond area, habitat heterogeneity and isolation. Oecologia 67:127–131

    Google Scholar 

  12. Delibes M, Gaona P, Ferreras P (2001) Effects of an attractive sink leading into maladaptive habitat selection. Am Nat 3:277–285

    Article  Google Scholar 

  13. Dhondt AA, Schillemans J(1983) Reproductive success of the great tit in relation to its territorial status. Anim Behav 31:902–912

    Google Scholar 

  14. Dobson FS, Oli MK (2001) The demographic basis of population regulation in Columbian Ground Squirrels. Am Nat 158:236–247

    Article  Google Scholar 

  15. Donázar JA (1987) Geographic variations in the diet of the Eagle Owls in Western Mediterranean Europe. In: Nero RW, Clark RJ, Knapton RJ, Hamre RH (eds) Biology and conservation of northern forest owl. General Technical Report RM-142. USDA, Fort Collins, pp 220–224

  16. Donázar JA (1988) Selección del hábitat de nidificación por el Buho real (Bubo bubo) en Navarra. Ardeola 35:233–245

    Google Scholar 

  17. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  18. Ens BJ, Kersten M, Brenninkmeijer A, Hulscher JB (1992) Territory quality, parental effort, and reproductive success of Oystercatchers (Haematopus ostralegus). J Anim Ecol 61:703–716

    Google Scholar 

  19. Ferrer M, Donázar JA (1996) Density-dependent fecundity by habitat heterogeneity in an increasing population of Spanish Imperial Eagles. Ecology 77:69–74

    Google Scholar 

  20. Fretwell SD, Lucas JHJ (1970) On territorial behaviour and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36

    Google Scholar 

  21. Frey H (1973) Zur Ökologie niederösterreichischer Uhupopulationen. Egretta 16:1–68

    Google Scholar 

  22. Goodburn SF (1991) Territory quality or bird quality? Factors determining breeding success in the Magpie Pica pica. Ibis 133:85–90

    Google Scholar 

  23. Harrison S, Taylor AD (1997) Empirical evidence for metapopulation dynamics. In: Hanski A, Gilpin ME (eds) Metapopulation biology. Academic, San Diego, pp 27–42

  24. Holt RD (1985) Population dynamics in two-patch environments: some anomalous consequences of an optimal habitat distribution. Theor Popul Biol 28:181–208

    Google Scholar 

  25. Kadmon R (1993) Population dynamic consequences of habitat heterogeneity: an experimental study. Ecology 74:816–825

    Google Scholar 

  26. Klomp H (1970) The determination of clutch size in birds: a review. Ardea 58:1–124

    Google Scholar 

  27. Kokko H, Sutherland WJ (1998) Optimal floating and queuing strategies: consequences for density dependence and habitat loss. Am Nat 152:354–366

    Article  Google Scholar 

  28. Komdeur J (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358:493–495

    Article  Google Scholar 

  29. Korpimäki E (1984) Population dynamics of birds of prey in relation to fluctuations in small mammal populations in western Finland. Ann Zool Fenn 21:287–293

    Google Scholar 

  30. Korpimäki E (1988) Effects of territory quality on occupancy, breeding performance and breeding dispersal in Tengmalm’s Owl. J Anim Ecol 57:97–108

    Google Scholar 

  31. Korpimäki E (1992) Diet composition, prey choice, and breeding success of long-eared owls: effects of multiannual fluctuations in food abundance. Can J Zool 70:2373–2381

    Google Scholar 

  32. Kotliar NB, Wiens JA (1990) Multiple scales of patchiness and patch structure: a hierarchical framework for the study of heterogeneity. Oikos 59:253–260

    Google Scholar 

  33. Krüger O, Lindstrom J (2001) Habitat heterogeneity affects population growth in goshawk Accipiter gentilis. J Anim Ecol 70:173–181

    Article  Google Scholar 

  34. Lack D (1966) Population studies of birds. Clarendon Press, Oxford

  35. Leditznig C (1992) Telemetric study in the Eagle Owl (Bubo bubo) in the foreland of the Alps in Lower Austria—methods and first results. Egretta 35:69–72

    Google Scholar 

  36. Leditznig C (1996) Habitatwahl des Uhus (Bubo bubo) im Südwesten Niederösterreichs und in den donaunahen Gebieten des Mühlviertels auf Basis radiotelemetrischer Untersuchungen. Abh Zool-Bot Ges Österreich 29:47–68

    Google Scholar 

  37. Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, London

  38. Marchesi L, Pedrini P, Sergio F (2002) Biases associated with diet study methods in the eagle owl. J Raptor Res 36:11–16

    Google Scholar 

  39. Martin TE (1987) Food as limit on breeding birds: a life-history perspective. Annu Rev Ecol Syst 18:453–487

    Article  Google Scholar 

  40. McPeek MA, Rodenhouse NL, Holmes RT, Sherry TW (2001) A general model of site-dependent population regulation: population-level regulation without individual-level interactions. Oikos 94:417–424

    Google Scholar 

  41. Mikkola H (1994) Eagle owl. In: Tucker GM, Heath MF (eds) Birds in Europe: their conservation status. Birdlife conservation series, vol. 3. Cambridge University Press, Cambridge, pp 326–327

  42. Morris DW (1988) Habitat-dependent population regulation and community structure. Evol Ecol 2:253–269

    Google Scholar 

  43. Morris DW (1991) Fitness and patch selection in white-footed mice. Am Nat 138:702–716

    Article  Google Scholar 

  44. Morris DW (1994) Habitat matching: alternatives and implications to populations and communities. Evol Ecol 8:387–406

    Google Scholar 

  45. Murdoch WW (1994) Population regulation in theory and practice. Ecology 75:271–287

    Google Scholar 

  46. Mysterud I, Dunker H (1982) Food and nesting ecology of the Eagle Owl, Bubo bubo (L.), in four neighbouring territories in Southern Norway. Viltrevy 12:71–113

    Google Scholar 

  47. Naveh Z, Lieberman A (1994) Landscape ecology. Theory and application. Springer, Berlin Heidelberg New York

  48. Oli MK, Dobson FS (2001) Population cycles in small mammals: the α hypothesis. J Mammal 82:573–581

    Google Scholar 

  49. Olsson V (1979) Studies of a population of eagle owls, Bubo bubo (L.), in southwest Sweden. Viltrevy 11:1–99

    Google Scholar 

  50. Ostfeld RS, Lidicker WZ Jr, Heske EJ (1985) The relationship between habitat heterogeneity, space use, and demography in a population of California voles. Oikos 45:433–442

    Google Scholar 

  51. Penteriani V (1996) The eagle owl (in Italian). Calderini Edagricole, Bologna

  52. Penteriani V (1997) Long-term study of a goshawk breeding population on a Mediterranean mountain (Abruzzi Apennines, Central Italy): density, breeding performances and diet. J Raptor Res 31:308–312

    Google Scholar 

  53. Penteriani V (2002) Variation in the function of the eagle owl vocal behaviour: territorial defence and intra-pair communication? Ethol Ecol Evol 14:275–281

    Google Scholar 

  54. Penteriani V (2003a) Breeding density affects the honesty of bird vocal displays as possible indicators of male/territory quality. Ibis 145:E127–E135

    Article  Google Scholar 

  55. Penteriani V (2003b) Simultaneous effects of age and territory quality on fecundity in Bonelli’s Eagle Hieraaetus fasciatus. Ibis 145:E77–E82

    Google Scholar 

  56. Penteriani V, Gallardo M, Cazassus H (2000) Diurnal vocal activity of young eagle owls and its implications in detecting occupied nests. J Raptor Res 34:232–235

    Google Scholar 

  57. Penteriani V, Gallardo M, Roche P, Cazassus H (2001) Effects of landscape spatial structure and composition on the settlement of the Eagle Owl Bubo bubo in a Mediterranean habitat. Ardea 89:331–340

    Google Scholar 

  58. Penteriani V, Gallardo M, Roche P (2002a) Landscape structure and food supply affect eagle owl Bubo bubo density and breeding performance: a case of intra-population heterogeneity. J Zool 257:365–372

    Article  Google Scholar 

  59. Penteriani V, Faivre B, Mazuc J, Cezilly F (2002b) Pre-laying vocal activity as a signal of male and nest stand quality in goshawks. Ethol Ecol Evol 14:9–17

    Google Scholar 

  60. Potapov ER (1997) What determines the population density and reproductive success of rough-legged buzzards, Buteo lagopus, in the Siberian tundra? Oikos 78:362–378

    Google Scholar 

  61. Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661

    Article  Google Scholar 

  62. Pulliam HR (2000) On the relationship between niche and distribution. Ecol Lett 3:349–361

    Article  Google Scholar 

  63. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  64. Ricklefs RE (1983) Avian demography. Curr Ornithol 1:1–32

    Google Scholar 

  65. Rodenhouse NL, Sherry TW, Holmes RT (1997) Site-dependent regulation of population size: a new synthesis. Ecology 78:2025–2042

    Google Scholar 

  66. Rodenhouse NL, Sherry TW, Holmes RT (1999) Multiple mechanisms of population regulation: contributions of site dependence, crowding, and age structure. In: Proceedings of international ornithological congress, vol 22, pp 2939–2952

  67. Roese JH, Risenhoover KL, Folse LJ (1991) Habitat heterogeneity and foraging efficiency: an individual-based model. Ecol Model 57:133–143

    Article  Google Scholar 

  68. Rosenzweig ML, Abramsky Z(1980) Microtine cycles: the role of habitat heterogeneity. Oikos 34:141–146

    Google Scholar 

  69. Sergio F, Newton I (2003) Occupancy as a measure of territory quality. J Anim Ecol 72:857–865

    Article  Google Scholar 

  70. Simmons RE, Avery DM, Avery G (1991) Biases in diets determined from pellets and remains: correction factors for a mammal and bird-eating raptor. J Raptor Res 25:63–67

    Google Scholar 

  71. Sokal RR, Rohlf FJ (1995) Biometry, the principles and practice of statistics in biological research. Freeman, New York

  72. Steenhof K (1987) Assessing raptor reproductive success and productivity. In: Pendleton G, Millsap BA, Cline KW, Bird DM (eds) Raptor management techniques manual. National Wildlife Federation, Washington, pp 157–170

  73. Steenhof K, Kochert MN, McDonald TL (1997) Interactive effects of prey and weather on golden eagle reproduction. J Anim Ecol 66:350–362

    Google Scholar 

  74. Steenhof K, Kochert MN, Carpenter LB, Lehman RN (1999) Long-term prairie falcon population changes in relation to prey abundance, weather, land uses, and habitat conditions. Condor 101:28–41

    Google Scholar 

  75. Strauss von MJ, Glück E (1995) Einfluß unterschiedlicher Habitatqualität auf Brutphänologie und Reproduktionserfolg bei Blaumeisen (Parus caeruleus). Vogelwarte 38:10–23

    Google Scholar 

  76. Sutherland WJ (1996) From individual behaviour to population ecology. Oxford University Press, Oxford

  77. Thiollay JM (1990) Comparative diversity of temperate and tropical forest bird communities: the influence of habitat heterogeneity. Acta Ecol 11: 887–911

    Google Scholar 

  78. Turner MG (1989) Landscape ecology: the effect of pattern on processes. Annu Rev Ecol Syst 20:171–197

    Article  Google Scholar 

  79. Virkkala R (1990) Ecology of the Siberian Tit Parus cinctus in relation to habitat quality: effects of forest management. Ornis Scand 21:139–146

    Google Scholar 

  80. Wauters LA, Dhondt AA (1990) Red squirrel (Sciurus vulgaris Linnaeus, 1758) population dynamics in different habitats. Z Säugetierkd 55:161–175

    Google Scholar 

  81. Wauters LA, Lens L (1995) Effects of food availability and density on red squirrel (Sciurus vulgaris) reproduction. Ecology 76:2460–2469

    Google Scholar 

  82. Weatherhead PJ, Robertson RJ (1977) Harem size, territory quality, and reproductive success in the redwinged blackbird (Agelaius phoeniceus). Can J Zool 55:1261–1267

    Google Scholar 

  83. Wiens JA (1976) Population responses to patchy environments. Annu Rev Ecol Syst 7:81–120

    Article  Google Scholar 

Download references

Acknowledgments

D. Becker, M. Forero, O. Krüger, M. Mönkkönen, N. L. Rodenhouse, T. Sota and three anonymous referees made a useful critique of the first draft of the manuscript. We thank P. Roche for helping with the IDRISI program, H. Magnin, C. Horisberger and P. Horisberger and O. Maubec for the logistic help during the fieldwork. During the study, V.P. received a research grant from the Regional Park of Luberon (France) and a post-doctoral grant from the Estación Biológica de Doñana (Consejo Superior de Investigaciones Científicas, Spain).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Vincenzo Penteriani.

Appendices

Appendix 1

Territory-specific yearly data of reproductive output (i.e. number of fledglings) of the French population of eagle owls during the 29 years of the study. The years 1973 and 1974 are absent because during this period it was impossible to collect data in the field (–, missing data). Mean number of fledglings, coefficient of reproduction (CV) and percentage of contributing pairs (%) per year was only presented for the 18 years shown in Fig. 1 and during which we were able to obtain data for at least ten territories each year (see details in Materials and methods)

Territories 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 CV Percentage
1971 2 3 2 2
1972 3 2 2 1
1975 2 2 2 2 2
1976 2 3
1977 2 2 1 3 2 2 1 1 2
1978 1 1 2 2 2 1 2 2 1 3 2 1.7 37.4 37.5
1979 2 2 2 1 2 3 3 1 1 1 1 1 1 0 1 2 2 2 1.5 50.3 35.3
1980 1 2 1 2 2 2 2 2 2 2 2 2 2 1 1 2 1 2 1 2 2 3 3 1 1.8 32.8 41.6
1981 1 1 2 1 1 2 2 1 2 1 2 1 1 2 1 2 2 1 3 2 1 1.5 39.6 38.1
1982 1 1 2 2 2 2 1 3 3 2 1 3 0 1 2 2 2 0 2 3 2 2 1.8 49 38.1
1983 1 2
1984 2 2 2 1 2 1 2 2 2 3 2 2 1 2 2 2 1 1 2 2 1 1 1.7 31.8 40.1
1985 3 1 2 2 2 2 1 1 2 1 1 2 1 2 0 2 1.6 46.6 40
1986 2 1 0 0 2 0 2 1 0 1 1 0.9 91.3 27.3
1987 1 0 2 0 0 1 2 2 3 2 1 2 1 2 2 1.4 65 33.3
1988 2 1 2 2 1 3 2 2 1 0 2 2 2 1.7 44.4 38.5
1989 2 2 2
1990 0 0 0 0 2 2 2 1 2 1 1 2 1 2 2 1.2 71.8 33.3
1991 2 1 2 2 2 2 3 2 1 3 2 2 2 3 3 2.1 30 40
1992 2 2 1 2 0 2 0 2 2 2 1.5 56.6 40
1993 0 1 3 2 2 2 2 3 1 0 1.6 67.1 40
1994 1 1 2 2 2 3 3 2 2 2 2 2 1 1 2 2 3 1 2 1 1.9 36.2 40
1995 2 3 2 3
1996 2 1 2 2 2 2 2 2 1 2 1 2 3 2 1 2 3 2 2 1.9 30 42.1
1997 2 0 2
1998 2 2 2 2 2 2 1 2 3 2 2 1 2 3 2 2 2 25.8 43.8
1999 1 2 2 2 2 2 0 2 2 1 0 2 0 1 2 3 1.5 59.6 40

Appendix 2

Raw data for the eight variables of landscape structure, diet and density (see Materials and methods for details) that we used to explain differences in mean reproductive output and its annual variance within the population. The results of the two forward stepwise multiple regression models that we performed using mean reproductive output and CV as dependent variables are summarised in Table 1

Territoriesa 1 2 4 6 7 9 10 11 12 13 16 18 19 29 30 32 34
Percentage of open country 19.4 29.4 30.3 26.1 29.6 22.3 60.5 38.4 49.5 74.5 43.1 31.5 12.5 55.1 53.1 45.1 26.9
Percentage of woodland 38.2 37.2 41.8 59.3 58.5 68.1 20.7 50.2 28.7 9.3 22.8 27.1 49.6 10.6 12.8 22.8 31.6
Number of ecotones 11.5 14.9 15.1 14.5 12.3 13.5 15.4 14.1 11.2 11.9 13.5 13.1 12.8 13.5 13.5 13.5 11.9
Shannon diversity index 1.7 1.9 1.9 1.6 1.6 1.4 1.9 1.8 2 1.8 2 2 1.6 2 2 2 1.8
NND (m) 800 780 1200 670 1,200 1,000 760 760 2,000 2,550 900 3,500 3,600 1,000 1,500 1,600 2,500
Diet richness 70 70 30 68 69 70 70 70 30 31 68 32 32 65 69 69 32
Diet diversity 2.3 2.3 1.9 2.3 2.3 2.2 2.2 2.1 1.9 1.9 2.1 1.9 1.9 2.3 2.3 2.3 1.9
Distance (m) from the nearest patch of open country 40.7 27.5 0.0 0.0 0.0 159.8 0.0 27.5 0.0 0.0 27.5 55.0 27.5 22.5 27.5 12.7 87.0
  1. aThe numbers identifying each territory correspond to the ones in Appendix 1

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Penteriani, V., Delgado, M.M., Gallardo, M. et al. Spatial heterogeneity and structure of bird populations: a case example with the eagle owl. Popul Ecol 46, 185–192 (2004). https://doi.org/10.1007/s10144-004-0178-8

Download citation

Keywords

  • Spatial heterogeneity
  • Territory quality
  • Breeding performance
  • Coefficient of variation
  • Bird populations
  • Eagle owl (Bubo bubo)