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Migratory decisions in birds: extent of genetic versus environmental control

  • Behavioral ecology - Original Paper
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Abstract

Migration is one of the most spectacular of animal behaviors and is prevalent across a broad array of taxa. In birds, we know much about the physiological basis of how birds migrate, but less about the relative contribution of genetic versus environmental factors in controlling migratory tendency. To evaluate the extent to which migratory decisions are genetically determined, we examined whether individual western burrowing owls (Athene cunicularia hypugaea) change their migratory tendency from one year to the next at two sites in southern Arizona. We also evaluated the heritability of migratory decisions by using logistic regression to examine the association between the migratory tendency of burrowing owl parents and their offspring. The probability of migrating decreased with age in both sexes and adult males were less migratory than females. Individual owls sometimes changed their migratory tendency from one year to the next, but changes were one-directional: adults that were residents during winter 2004–2005 remained residents the following winter, but 47% of adults that were migrants in winter 2004–2005 became residents the following winter. We found no evidence for an association between the migratory tendency of hatch-year owls and their male or female parents. Migratory tendency of hatch-year owls did not differ between years, study sites or sexes or vary by hatching date. Experimental provision of supplemental food did not affect these relationships. All of our results suggest that heritability of migratory tendency in burrowing owls is low, and that intraspecific variation in migratory tendency is likely due to: (1) environmental factors, or (2) a combination of environmental factors and non-additive genetic variation. The fact that an individual’s migratory tendency can change across years implies that widespread anthropogenic changes (i.e., climate change or changes in land use) could potentially cause widespread changes in the migratory tendency of birds.

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References

  • Adriaensen F, Dhondt AA (1990) Population dynamics and partial migration of the European robin (Erithacus rubecula) in different habitats. J Anim Ecol 59:1077–1090

    Article  Google Scholar 

  • Adriaensen F, Dhondt AA, Matthysen E (1990) Bird migration. Nature 347:23

    Article  Google Scholar 

  • Archaux F (2003) Birds and climate change. Life Environ 53:33–41

    Google Scholar 

  • Bell CP (2005) Inter- and intrapopulation migration patterns. Ideas, evidence, and research priorities. In: Greenberg R, Marra PP (eds) Birds of two worlds. The ecology and evolution of migration. Johns Hopkins University Press, Baltimore, pp 44–52

    Google Scholar 

  • Berthold P (1984) The control of partial migration in birds: a review. Ring 10:253–265

    Google Scholar 

  • Berthold P (1988) Evolutionary aspects of migratory behavior in European warblers. J Evol Biol 1:195–209

    Article  Google Scholar 

  • Berthold P (1991) Genetic control of migratory behaviour in birds. Trends Ecol Evol 6:254–257

    Article  Google Scholar 

  • Berthold P (2001) Bird migration: a general survey, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Berthold P, Helbig AJ (1992) The genetics of bird migration—stimulus, timing, and direction. Ibis 134(Suppl 1):35–40

    Google Scholar 

  • Berthold P, Pulido F (1994) Heritability of migratory activity in a natural bird population. Proc R Soc Lond B 257:311–315

    Article  Google Scholar 

  • Berthold P, Querner U (1981) Genetic basis of migratory behavior in European warblers. Science 212:77–79

    Article  PubMed  Google Scholar 

  • Berthold P, Mohr G, Querner U (1990) Steuerung und potentielle Evolutionsgeschwindigkeit des obligaten Teilzieherverhaltens: ergebniesse eines Zweiweg-Selektionsexperiments mit der Monchsgrasmucke (Sylvia atricapilla). J Ornithol 131:33–45

    Article  Google Scholar 

  • Biebach H (1983) Genetic determination of partial migration in the European robin (Erithacus rubecula). Auk 100:601–606

    Google Scholar 

  • Bock CE, Lepthien LW (1976) Synchronous eruptions of boreal seed-eating birds. Am Nat 110:559–571

    Article  Google Scholar 

  • Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83

    Article  PubMed  CAS  Google Scholar 

  • Boyle WA, Conway CJ (2007) Why migrate? A test of the evolutionary precursor hypothesis. Am Nat 169:344–359

    Article  PubMed  Google Scholar 

  • Conway CJ, Ellis LA (2004) Demography of burrowing owls nesting in urban and agricultural lands in southern Arizona. Report to Arizona Game and Fish Department. Wildlife research report no. 03-2004, US Geological Survey, Arizona Cooperative Fish and Wildlife Research Unit, Tucson, AZ

  • Conway CJ, Ogonowski MS (2005) Determining migratory status of burrowing owls in the Tucson Basin. Final Report to Arizona Bird Conservation Initiative. Wildlife research report no. 2005-06, US Geological Survey, Arizona Cooperative Fish and Wildlife Research Unit, Tucson, AZ

  • Conway CJ, Ellis LA, Rogne M (2005) Ecological and migratory status of burrowing owls nesting at Casa Grande Ruins National Monument and surrounding agricultural areas. Wildlife research report no. 2005-08. US Geological Survey, Arizona Cooperative Fish and Wildlife Research Unit, Tucson, AZ

  • Conway CJ, Garcia V, Smith MD, Ellis LA, Whitney J (2006) Comparative demography of burrowing owls within agricultural and urban landscapes in southeastern Washington. J Field Ornithol 77:280–290

    Article  Google Scholar 

  • Coppack T, Both C (2002) Predicting life-cycle adaptation of migratory birds to global climate change. In: Both C, Piersma T (eds) The avian calendar: exploring biological hurdles in the annual cycle. Proceedings of the 3rd Conference of the European Ornithologists Union, Groningen, August 2001. Ardea 90:369–378

  • Coppack T, Pulido F, Czisch M, Auer DP, Berthold P (2003) Photoperiodic response may facilitate adaptation to climatic change in long-distance migratory birds. Proc R Soc Lond B Suppl 270:S43–S46

    Article  Google Scholar 

  • Coulombe HN (1971) Behavior and population ecology of the burrowing owl, Speotyto cunicularia, in the Imperial Valley of California. Condor 73:162–176

    Article  Google Scholar 

  • Cristol DA, Baker MB, Carbone C (1999) Differential migration revisited. Latitudinal segregation by age and sex class. In: Nolan V, Ketterson ED, Thompson CF (eds) Current ornithology, vol 15. Kluwer, New York, pp 33–88

    Google Scholar 

  • Dhondt AA (1983) Variations in the number of overwintering stonechats possibly caused by natural selection. Ring Migr 4:155–158

    Google Scholar 

  • Enemar A, Nilsson L, Sjostrand B (1984) The composition and dynamics of the passerine bird community in a subalpine birch forest, Swedish Lapland. A 20-year study. Ann Zool Fenn 21:321–338

    Google Scholar 

  • Fiedler W (2003) Recent changes in migratory behavior of birds: a compilation of field observations and ringing data. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin, pp 21–38

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Garcia V, Conway CJ (2009a) Use of video probe does not affect burrowing owl reproductive parameters or return rates. J Wildl Manage 731):154–157

    Google Scholar 

  • Garcia V, Conway CJ (2009b) What constitutes a nesting attempt? Variation in criteria causes bias and hinders comparisons across studies. Auk 126(1):31–40

    Google Scholar 

  • Garcia V, Conway CJ, Ellis LA (2007) Protocols for estimating burrowing owl reproductive parameters based on data recorded during repeated visits to occupied burrows. Wildlife research report no. 2007-06. USGS Arizona Cooperative Fish and Wildlife Research Unit, Tucson, AZ

  • Gauthreaux SA (1982) The ecology and evolution of avian migration systems. In: Farner DS, King JR, Parkes KC (eds) Avian Biology 6. Academic Press, New York, pp 93–168

    Google Scholar 

  • Gienapp P, Visser ME (2006) Possible fitness consequences of experimentally advanced laying dates in great tits: differences between populations in different habitats. Funct Ecol 20:180–185

    Article  Google Scholar 

  • Hagen Y (1969) Norwegian studies on the reproduction of birds of prey and owls in relation to micro-rodent population fluctuations. Fauna 22:73–126

    Google Scholar 

  • Harper D (1985) Pairing strategies and mate choice in female robins (Erithacus rubecula). Anim Behav 33:862–875

    Article  Google Scholar 

  • Haug EA, Millsap BA, Martell MS (1993) Burrowing owl (Speotyto cunicularia). In: Poole A, Gill F (eds) The birds of North America, no. 61. The Academy of Natural Sciences, Philadelphia, pp 1–20

    Google Scholar 

  • Helbig AJ (1991) Experimental and analytical techniques used in bird orientation research. In: Berthold P (ed) Orientation in birds. Birkhauser, Basel, pp 270–306

    Google Scholar 

  • Helms B (2006) Zugunruhe of migratory and non-migratory birds in a circannual context. J Avian Biol 37:533–540

    Article  Google Scholar 

  • Hochachka WM, Wells JV, Rosenberg KV, Tessaglia-Hymes DL, Dhondt AA (1999) Irruptive migration of common redpolls. Condor 101:195–204

    Article  Google Scholar 

  • Intergovernmental Panel on Climate Change (ed) (2007) Climate change 2007: the physical science basis. Summary for policymakers. IPCC Secretariat, Geneva

    Google Scholar 

  • Jaksic FM, Jimenez JE, Castro SA, Feinsinger P (1992) Numerical and functional response of predators to a long-term decline in mammalian prey at a semi-arid Neotropical site. Oecologia 89:90–101

    Article  Google Scholar 

  • Kaitala A, Kaitala V, Lundberg P (1993) A theory of partial migration. Am Nat 142:59–81

    Article  Google Scholar 

  • Ketterson ED, Nolan V Jr (1976) Geographic variation and its climatic correlates in the sex ratio of eastern-wintering dark-eyed juncos (Junco hyemalis hyemalis). Ecology 57:679–693

    Article  Google Scholar 

  • Klute DS, Ayers LW, Green MT, Howe WH, Jones SL, Shaffer JA, Sheffield SR, Zimmerman TS (2003) Status assessment and conservation plan for the western burrowing owl in the United States. Biological technical publication FWS/BTP-R6001-2003. US Department of Interior, Fish and Wildlife Service, Washington, DC

  • Koenig WD, Knops JMH (2001) Seed crop size and eruptions of North American boreal seed-eating birds. J Anim Ecol 70:609–620

    Article  Google Scholar 

  • Korpimaki E (1986) Gradients in population fluctuations of Tengmalm’s owl Aegolius funereus in Europe. Oecologia 69:195–201

    Article  Google Scholar 

  • Korpimaki E (1987) Selection for nest-hole shift and tactics of breeding dispersal in Tengmalm’s owl Aegolius funereus. J Anim Ecol 56:185–196

    Article  Google Scholar 

  • Korpimaki E, Norrdahl K (1991) Numerical and functional responses of kestrels, short-eared owls and long-eared owls to vole densities. Ecology 72:814–825

    Article  Google Scholar 

  • Lack D (1943) The problem of partial migration. Br Birds 37:122–130

    Google Scholar 

  • Lack D (1944) The problem of partial migration (concluded). Br Birds 37:143–150

    Google Scholar 

  • Lack D (1968) Bird migration and natural selection. Oikos 19:1–9

    Article  Google Scholar 

  • Lundberg P (1988) The evolution of partial migration in birds. Trends Ecol Evol 3:172–175

    Article  Google Scholar 

  • Martin DJ (1973) Selected aspects of burrowing owl ecology and behavior. Condor 75:446–456

    Article  Google Scholar 

  • National Oceanic and Atmospheric Association (2007) National Weather Service Internet Services Team. Monthly precipitation for Tucson, Arizona. <http://www.wrh.noaa.gov/twc/climate/reports.php>. Accessed 17 November 2007

  • Newton I (1985) Lifetime reproductive output of female sparrowhawks. J Anim Ecol 54:241–253

    Article  Google Scholar 

  • Newton I (2006) Advances in the study of irruptive migration. Ardea 94:433–460

    Google Scholar 

  • Newton I, Marquiss M (1983) Dispersal of sparrowhawks between birthplace and breeding place. J Anim Ecol 52:463–477

    Article  Google Scholar 

  • Nice MM (1937) Studies in the life history of the Song sparrow, I. Trans Linn Soc NY 4:1–247

    Google Scholar 

  • Ogonowski MS (2007) Factors influencing migratory decisions of western burrowing owls. M.S. thesis, School of Natural Resources, University of Arizona, Tucson, AZ

  • Ogonowski MS, Conway CJ (2006) Migratory status and factors influencing winter residency of burrowing owls in southern Arizona. Final report to Arizona Bird Conservation Initiative. US Geological Survey, Arizona Cooperative Fish and Wildlife Research Unit, Tucson, AZ

  • Poulin RG, Wellicome TI, Todd LD (2001) Synchronous and delayed numerical responses of a predatory bird community to a vole outbreak on the Canadian prairies. J Raptor Res 35:288–295

    Google Scholar 

  • Pulido F, Berthold P, van Noordwijk AJ (1996) Frequency of migrants and migratory activity are genetically correlated in a bird population: evolutionary implications. Proc Natl Acad Sci 93:14642–14647

    Article  PubMed  CAS  Google Scholar 

  • Sandell M, Smith HG (1991) Dominance, prior occupancy, and winter residency in the great tit (Parus major). Behav Ecol Sociobiol 29:147–152

    Article  Google Scholar 

  • Schwabl H (1983) Auspragung und Bedeutung des Teilzugverhaltnes iener sudwestdeutschen Population der Amsel Turdus merula. J Ornithol 124:101–116

    Article  Google Scholar 

  • Smith MD, Conway CJ (2007) Use of mammal manure by nesting burrowing owls: a test of four functional hypotheses. Anim Behav 73:65–73

    Article  Google Scholar 

  • Smith HG, Nilsson J-A (1987) Intraspecific variation in migratory pattern of a partial migrant, the blue tit (Parus caeruleus): an evaluation of different hypotheses. Auk 104:109–115

    Google Scholar 

  • Sonerud GA, Solheim R, Prestrud K (1988) Dispersal of Tengmalm’s owl Aegolius funereus in relation to prey availability and nesting success. Ornis Scand 19:175–181

    Article  Google Scholar 

  • SPSS (2006) Version 15.0 for Windows. SPSS, Chicago

    Google Scholar 

  • Sutherland WJ (1998) Evidence for flexibility and constraint in migration systems. J Avian Biol 29:441–446

    Article  Google Scholar 

  • Terrill SB (1987) Social dominance and migratory restlessness in the dark-eyed junco (Junco hyemalis). Behav Ecol Socio 21:1–11

    Article  Google Scholar 

  • Terrill SB, Able KP (1988) Bird migration terminology. Auk 105:205–206

    Google Scholar 

  • Turner RM, Brown DE (1994) Sonoran desertscrub. In: Brown DE (ed) Biotic communities. Southwestern United States and northwestern Mexico. University of Utah Press, Salt Lake City, pp 181–221

    Google Scholar 

  • van Noordwijk AJ, Pulido F, Helm B, Coppack T, Delingat J, Dingle H, Hedenstrom A, van der Jeugd H, Marchetti C, Nilsson A, Perez-Tris J (2006) A framework for the study of genetic variation in migratory behavior. J Ornithol 147:221–233

    Article  Google Scholar 

  • Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172

    Article  PubMed  Google Scholar 

  • Wiggins DA, Holt DW, Leasure SM (2006) Short-eared Owl (Asio flammeus). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. <http://bna.birds.cornell.edu.bnaproxy.birds.cornell.edu/bna/species/062 doi:10.2173/bna.62> Accessed 5 November 2008

  • Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Modeling, estimation, and decision making. Academic Press, San Diego

    Google Scholar 

  • Winkler DW (2005) How do migration and dispersal interact? In: Greenberg R, Marra PP (eds) Birds of two worlds. The ecology and evolution of migration. Johns Hopkins University Press, Baltimore, pp 401–413

    Google Scholar 

  • Winkler DW, Dunn PO, McCulloch CE (2002) Predicting the effects of climate change on avian life history traits. Proc Natl Acad Sci 99:13595–13599

    Article  PubMed  CAS  Google Scholar 

  • Wormworth J, Mallon K (2006) Bird species and climate change: the global status report. Report prepared for the World Wide Fund for Nature, Gland, Switzerland

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Acknowledgments

The National Fish and Wildlife Foundation, United States Environmental Protection Agency, Arizona Bird Conservation Initiative, Arizona Game and Fish Department, the University of Arizona, and the United States Department of Defense provided financial support. Casa Grande Ruins National Monument provided housing and a vehicle. Davis-Monthan Air Force Base and Tucson Electric Park facilitated access to burrowing owl nests on their respective facilities. M. Borgstrom provided statistical expertise. L. Ellis, A. Estergard, J. Horst, S. Humphrey, M. Lefebvre, R. Richardson, S. Robinson, E. Wert, and K. Wright helped collect data in the field. M. Culver provided advice on approaches for estimating and discussing heritability. M. Culver, R. W. Mannan, R. J. Steidl, P. Banks, and two anonymous reviewers provided comments that improved the manuscript. This study complies with all current laws of the United States of America.

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Correspondence to Mark S. Ogonowski.

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Communicated by Peter Banks.

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Ogonowski, M.S., Conway, C.J. Migratory decisions in birds: extent of genetic versus environmental control. Oecologia 161, 199–207 (2009). https://doi.org/10.1007/s00442-009-1356-3

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