Journal of Ornithology

, Volume 147, Issue 2, pp 212–220 | Cite as

Animal migration: is there a common migratory syndrome?

Review

Abstract

Ornithologists, and especially northern hemisphere ornithologists, have traditionally thought of migration as an annual return movement of populations between regular breeding and non-breeding grounds. Problems arise because selection does not ordinarily act on populations and because organisms of many taxa (including birds) are clearly migrants, but fail to undertake movements of the kind described. There are also extensive return movements that are not migratory. I propose that it is more useful to think of migration as a syndrome of behavioral and other traits that function together within individuals, and that such a syndrome provides a common ground across taxa from aphids to albatrosses. Large-scale return movements of populations are one outcome of the syndrome. Similar behavioral and physiological traits serve both to define migration and to provide a test for it. I use two insect (Hemipteran) examples to illustrate migratory syndromes and to demonstrate that, in many migrants, behavior and physiology correlate with life history and morphological traits to form syndromes at two levels. I then compare the two Hemipterans with migration in birds, butterflies, and fish to assess the question of whether there are migratory syndromes in common between these diverse migrants. Syndromes are more similar at the level of behavior than when morphology and life history traits are included. Recognizing syndromes leads to important evolutionary questions concerning migration strategies, trade-offs, the maintenance of genetic variance and the responses of migratory syndromes to both similar and different selective regimes.

Keywords

Behavior Evolution Life histories Migration Syndromes 

Notes

Acknowledgments

This paper is based on a plenary talk at the European Science Foundation conference on ‘Migration in the life-history of birds’ in Wilhelmshaven, Germany in February 2005. I am grateful to Franz Bairlein for the invitation to speak and to the ESF for travel support to attend. Scott Carroll provided much background information and valuable discussion on soapberry bugs and read the first draft of the manuscript. Thoughtful and detailed comments by Alistair Drake did much to clarify and improve the final version. My own research on migration has been supported by the US National Science Foundation and by an Alexander v. Humboldt Senior Scientist Award at the Vogelwarte Radolfzell hosted by Peter Berthold.

References

  1. Able KP (1997) Review of H Dingle, migration: the biology of life on the move. Anim Behav 53:437–438CrossRefGoogle Scholar
  2. Alerstam T, Hedenström A, Åkesson S (2003) Long-distance migration: evolution and determinants. Oikos 103:247–260CrossRefGoogle Scholar
  3. Arnold GP (1981) Movements of fish in relation to water currents. In: Aidley DJ (ed) Animal migration. Cambridge University Press, Cambridge, pp 55–80Google Scholar
  4. Bairlein F (2003) Nutritional strategies in migratory birds. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 321–332Google Scholar
  5. Berthold P, Gwinner E, Sonnenshein E (2003) Avian migration. Springer, Berlin Heidelberg New YorkGoogle Scholar
  6. Böhning-Gaese K, Halbe B, Lemoine N, Oberrath R (2000) Factors influencing clutch size, number of broods and annual fecundity in North American and European birds. Evol Ecol Res 2:823–829Google Scholar
  7. Bradshaw WE (1986) Pervasive themes in insect life cycle strategies. In: Taylor F, Karban R (eds) The evolution of insect life cycles. Springer, New York Berlin Heidelberg, pp 261–275Google Scholar
  8. Butler PJ, Bishop CM, Woakes AJ (2003) Chasing a wild goose: posthatch growth of locomotor muscles and behavioural physiology of migration of an Arctic goose. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 527–542Google Scholar
  9. Carroll SP, Boyd C (1992) Host race radiation in the soapberry bug: natural history with the history. Evolution 46:1052–1069CrossRefGoogle Scholar
  10. Carroll SP, Marler M, Winchell R, Dingle H (2003) Evolution of cryptic flight morph and life history differences during host race radiation in the soapberry bug, Jadera haematoloma Herrich-Schaeffer (Hemiptera: Rhopalidae). Ann Ent Soc Am 96:135–143CrossRefGoogle Scholar
  11. Cornelius JM, Katti M, Hahn TP (2005) Temporal patterns of fat deposition, hematocrit and plumage moult in an irruptive nomad, the red crossbill Loxia curvirostra. European science foundation conference “Migration in the life-history of birds”, Wilhelmshaven Germany, Programme p 35 (Abstract)Google Scholar
  12. Dingle H (1996) Migration: the biology of life on the move. Oxford University Press, New YorkGoogle Scholar
  13. Dingle H (2001) The evolution of migratory syndromes in insects. In: Woiwood IP, Reynolds DR, Thomas CD (eds) Insect movement: mechanisms and consequences, CABI Publishing, Oxford, pp 159–181Google Scholar
  14. Dingle H (2002) Hormonal mediation of insect life histories. In: Pfaff R et al (eds) Hormones, Brain and behavior, vol 3, Elsevier Science, New York, pp237–279Google Scholar
  15. Dingle H, Winchell R (1997) Juvenile hormone as a mediator of plasticity in insect life histories. Arch Insect Biochem Physiol 35:359–373CrossRefGoogle Scholar
  16. Dingle H, Zalucki MP, Rochester WA (1999) Season-specific directional movement in migratory Australian butterflies. Aust J Entomol 38:323–329CrossRefGoogle Scholar
  17. Elliott JM (1988) Growth, size, biomass and production in contrasting populations of trout Salmo trutta in two lake district streams. J Anim Ecol 57:49–60CrossRefGoogle Scholar
  18. Fontaine M (1975) Physiological mechanisms in the migration of marine and amphihaline fish. Adv Mar Biol 13:241–355CrossRefGoogle Scholar
  19. Fraser DJ, Bernatchez L (2005) Adaptive migratory divergence among sympatric brook char populations. Evolution 59:611–624PubMedGoogle Scholar
  20. Frazzetta T (1975) Complex adaptations in evolving populations. Sinauer, Sunderland, Mass.Google Scholar
  21. Gatehouse AG (1987) Migration: a behavioural process with ecological consequences?. Antenna 11:10–12Google Scholar
  22. Gwinner E, Helm B (2003) Circannual and circadian contributions to the timing of avian migration. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 81–95Google Scholar
  23. Hedenström A, Alerstam T, Åkesson S (eds) (2003) Ecology of long-distance movements: migration and orientation. Oikos 103:243–448Google Scholar
  24. Helbig A (2003) Evolution of bird migration. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 3–20Google Scholar
  25. Hockey PAR, Leseberg A, Loewenthal D (2003) Dispersal and migration of juvenile African black oystercatchers Haematopus moquini. Ibis 145:512, (Electronic Ibis 145:E114–E123)CrossRefGoogle Scholar
  26. Jander R (1975) Ecological aspects of spatial orientation. Annu Rev Ecol Syst 6:171–188CrossRefGoogle Scholar
  27. Jones PJ (1989) General aspects of quelea migrations. In: Bruggers RL, Elliott CCH (eds) Quelea quelea: Africa’s bird pest. Oxford University Press, Oxford, pp 102–112Google Scholar
  28. Jouventin P, Weimerskirch H (1990) Satellite tracking of wandering albatrosses. Nature 343:746–748CrossRefGoogle Scholar
  29. Kennedy JS (1966) Nervous co-ordination of instincts. Camb Res 2:29–32Google Scholar
  30. Kennedy JS (1985) Migration, behavioral and ecological. In: Rankin MA (ed) Migration: mechanisms and adaptive significance. Contrib Mar Sci 27(Suppl):5–26Google Scholar
  31. Kennedy JS, Booth CO (1963a) Free flight of aphids in the laboratory. J Exp Biol 40:67–85Google Scholar
  32. Kennedy JS, Booth CO (1963b) Co-ordination of successive activities in an aphid The effect of flight on settling responses. J Exp Biol 40:351–369Google Scholar
  33. Kennedy JS, Booth CO (1964) Co-ordination of successive activities in an aphid Depression of settling after flight. J Exp Biol 41:805–824PubMedGoogle Scholar
  34. Kennedy JS, Ludlow AR (1974) Co-ordination of two kinds of flight activity in an aphid. J Exp Biol 61:173–196PubMedGoogle Scholar
  35. Kennedy JS, Booth CO, Kershaw WJS (1961) Host finding by aphids in the field III Visual attraction. Ann Appl Biol 49:1–21CrossRefGoogle Scholar
  36. Ketterson ED, Nolan V Jr (1999) Adaptation, exaptation and constraint: a hormonal perspective. Am Nat 154(Suppl):S4–S25CrossRefGoogle Scholar
  37. Leisler B, Winkler H (2003) Morphological consequences of migration in passerines. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 175–186Google Scholar
  38. Newton I (2003) Geographical patterns in bird migration. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 211–224Google Scholar
  39. Newton I (2005) Stopover ecology, migration-related mortality and population limitation in birds. European science foundation conference “Migration in the life-history of birds” Wilhelmshaven, Germany, Programme p 8 (Abstract)Google Scholar
  40. van Noordwijk AJ, Pulido F, Helm B, Coppack T, Delingat J, Dingle H, Hedenström A, van der Jeugd H, Marchetti C, Nilsson A, Pērez-Tris J (2006) A framework for the study of genetic variation in migratory behaviour. J Ornithol (in press)Google Scholar
  41. Pulido F, Berthold P (2003) Quantitative genetic analysis of migratory behaviour. In: Berthold P, Gwinner E, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 53–77Google Scholar
  42. Rankin MA (1978) Hormonal control of insect migratory behavior. In: Dingle H (eds) The evolution of insect migration and diapause. Springer, New York Berlin Heidelberg, pp 5–32Google Scholar
  43. Rankin MA (1991) Endocrine effects on migration. Am Zool 31:217–230Google Scholar
  44. Ricklefs RE (2000a) Lack, Skutch, and Moreau: the early development of life-history thinking. Condor 102:3–8CrossRefGoogle Scholar
  45. Ricklefs RE (2000b) Density dependence, evolutionary optimization, and the diversification of avian life-histories. Condor 102:9–22CrossRefGoogle Scholar
  46. Roff D (1991) Life history consequences of bioenergetic and biomechanical constraints on migration. Am Zool 31:205–215Google Scholar
  47. Schaefer T, Pulido F (2005) Clutch size determination in short-distance and long-distance migrants. European science foundation conference “Migration in the life-history of birds” Wilhelmshaven Germany, Programme p 46 (Abstract)Google Scholar
  48. Schaffer WM, Elson PF (1975) The adaptive significance of variations in life history among local populations of Atlantic salmon in North America. Ecology 56:577–590CrossRefGoogle Scholar
  49. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277PubMedCrossRefGoogle Scholar
  50. Slansky F (1980) Food consumption and reproduction as affected by tethered flight in female milkweed bugs (Oncopeltus fasciatus). Entomol Exp Appl 28:277–286CrossRefGoogle Scholar
  51. Snyder RJ, Dingle H (1989) Adaptive, genetically based differences in life history between estuary and freshwater threespine sticklebacks (Gasterosteus aculeatus L). Can J Zool 67:2448–2454CrossRefGoogle Scholar
  52. Spieth HR, Cordes R-G, Dorka M (1998) Flight directions in the migratory butterfly Pieris brassicae: results from semi-natural experiments. Ethology 104:339–352CrossRefGoogle Scholar
  53. Srygley RB, Oliveira EG (2001) Orientation mechanisms and migration strategies within the flight boundary layer. In: Woiwood IP, Reynolds DR, Thomas CD (eds) Insect movement: mechanisms and consequences. CABI Publishing, Oxford, pp 183–206Google Scholar
  54. Winchell R, Dingle H, Moyes CD (2000) Enzyme profiles in two wing polymorphic soapberry bug populations (Jadera haematoloma Rhoplaidae). J Insect Physiol 46:1365–1373CrossRefPubMedGoogle Scholar
  55. Wingfield JC (2003) Avian migration: regulation of facultative-type movements. In: Berthold P, Gwinner G, Sonnenshein E (eds) Avian migration. Springer, Berlin Heidelberg New York, pp 113–125Google Scholar
  56. Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–231CrossRefPubMedGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2006

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of CaliforniaDavisUSA
  2. 2.School of Integrative BiologyUniversity of QueenslandBrisbaneAustralia

Personalised recommendations