Behavioral Ecology and Sociobiology

, Volume 59, Issue 1, pp 44–50 | Cite as

Differential predator escape performance contributes to a latitudinal sex ratio cline in a migratory shorebird

  • Silke NebelEmail author
  • Ronald C. Ydenberg
Original Article


Sexual segregation outside the mating season is common in vertebrates, and has been attributed to sexual differences in predator escape performance in ungulates and fish, but not in birds. Here, we tested the hypothesis that sex- and latitude-specific predator escape performance underlies the differential nonbreeding distribution of western sandpipers (Calidris mauri), a migratory shorebird. Females overwinter further south along the American Pacific coast, creating a latitudinal cline in sex ratio. Escape performance is reduced with increasing body mass, and birds generally carry less fat further south. Western sandpipers with poor escape performance were therefore predicted to prefer southern sites to reduce the risk of mortality posed by predators. Data from four nonbreeding latitudes showed that wing loading, used as an index of escape performance, was overall higher for females, and that it decreased with latitude in both sexes. Within latitudes, wing loading was lower at smaller, and presumably more dangerous, sites. Flight response to a predatory attack was longer in the south. Mortality risk offers a novel and candidate explanation for differential distribution patterns in western sandpipers and possibly other avian migrants.


Differential migration Mortality risk Predation danger Sex ratio cline Western sandpiper 



Logistical help was received from Bodega Bay Marine Lab, California; Craig Sasser at USFWS, Cape Romain NWR, South Carolina; Gilberto Salomon, Patolandia Hunting Club, Mexico; John Christy at the Smithsonian Tropical Research Institute, Panama, and the Canadian Wildlife Service. John Takekawa and Nils Warnock provided the 2003 wing loading data from San Francisco Bay. We thank Guillermo Fernandez for facilitating work in Mexico. Cadi Schiffer, John Takekawa, and Nils Warnock assisted with field work in California; Virgilio Antonio Pérez in Mexico; and Deborah Buehler in Panama. Dov Lank, Nils Warnock, and Tony Williams provided valuable comments on the manuscript. Financial support was received from the Government of Canada, Centre of Wildlife Ecology/Simon Fraser University and Sigma Xi, The Scientific Research Society


  1. Berthold P (1996) Control of bird migration. Chapman & Hall, LondonGoogle Scholar
  2. Bertochi LE, Castro G, Myers JP (1984) Notes on the predators, especially the peregrine, of sanderlings on the Peruvian coast. Wader Study Group Bull 42:31–32Google Scholar
  3. Bonenfant C, Loe LE, Mysterud A, Langvatn R, Stenseth NC, Gaillard J-M, Klein F (2004) Multiple causes of sexual segregation in European red deer: enlightenments from varying breeding phenology at high and low latitude. Proc R Soc Lond B 271:883–892CrossRefGoogle Scholar
  4. Buchanan JB (1996) A comparison of behavior and success rates of merlins and peregrine falcons when hunting dunlins in two coastal habitats. J Raptor Res 30:93–98Google Scholar
  5. Buchanan JB, Schick CT, Brennan LA, Herman SG (1988) Merlin predation on wintering Dunlins: hunting success and Dunlin escape tactics. Wilson Bull 100:108–118Google Scholar
  6. Burns JG, Ydenberg RC (2002) The effects of wing loading and gender on the escape flights of least sandpipers (Calidris minutilla) and western sandpipers (Calidris mauri). Behav Ecol Sociobiol 52:128–136CrossRefGoogle Scholar
  7. Cristol DA, Baker MB, Carbone C (1999) Differential migration revisited: latitudinal segregation by age and sex class. Curr Ornithol 15:33–88Google Scholar
  8. Davidson NC (1984) Survival of shorebirds (Charadrii) during severe weather: the role of nutritional reserves. In: Burger J, Olla BL (eds) Shorebirds: migration and foraging behavior, vol 6. Plenum, New York, pp 231–249Google Scholar
  9. Dekker D (1998) Over-ocean flocking by Dunlins, Calidris alpina, and the effect of raptor predation at Boundary Bay, British Columbia. Can Field Nat 112:694–697Google Scholar
  10. Dekker D, Ydenberg R (2004) Raptor predation on wintering Dunlins in relation to the tidal cycle. Condor 106:415–419CrossRefGoogle Scholar
  11. Dierschke V (2003) Predation hazard during migratroy stopover: are light or heavy birds under risk? J Avian Biol 34:24–29CrossRefGoogle Scholar
  12. Erritzoe J, Fuller R (1999) Sex differences in winter distribution of Long-eared Owls (Asio otus) in Denmark and neighbouring countries. Vogelwarte 40:80–87Google Scholar
  13. Gauthreaux SA, Jr (1978) The ecological significance of behavioral dominance. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology, vol 3. Plenum, New York, pp 17–54Google Scholar
  14. Guglielmo CG, Burns JG (2001) Avian forensics: predicting body fat and body mass from wing remains. J Avian Biol 32:198–203CrossRefGoogle Scholar
  15. 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 57:679–693CrossRefGoogle Scholar
  16. Koolhaas A, Dekinga A, Piersma T (1993) Disturbance of foraging Knots by aircraft in the Dutch Wadden Sea in August–October 1992. Wader Study Group Bull 68:20–22Google Scholar
  17. Kullberg C (1998) Does diurnal variation in body mass affect take-off ability in wintering willow tits? Anim Behav 56:227–233CrossRefPubMedGoogle Scholar
  18. Kullberg C, Jakobsson S, Fransson T (1998) Predator-induced take-off strategy in great tits (Parus major). Proc R Soc Lond B 265:1659–1664CrossRefGoogle Scholar
  19. Kullberg C, Jakobsson S, Fransson T (2000) High migratory fuel loads impair predator evasion in Sedge Warblers. Auk 117:1034–1038CrossRefGoogle Scholar
  20. Lank DB, Ydenberg RC (2003) Death and danger at migratory stopovers: problems with “predation risk”. J Avian Biol 34:225–228CrossRefGoogle Scholar
  21. Lank DB, Butler RW, Ireland J, Ydenberg RC (2003) Effects of predation danger on migration strategies of sandpipers. Oikos 103:303–319CrossRefGoogle Scholar
  22. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640Google Scholar
  23. Lind J, Fransson T, Jakobsson S, Kullberg C (1999) Reduced take-off ability in robins (Erithacus rubecula) due to migratory fuel load. Behav Ecol Sociobiol 46:65–70CrossRefGoogle Scholar
  24. Lindström Å (1989) Finch flock size and risk of hawk predation at a migratory stopover site. Auk 106:225–232Google Scholar
  25. Lissimore D, Lemon M, Lank DB, Butler RW, Ydenberg RC (1999) Large and consistent body mass differences of migrant calidris sandpipers at adjacent stopover sites: phenomenon and possible explanations. Wader Study Group Bull 88:55–58Google Scholar
  26. Lovvorn JR (1994) Nutrient reserves, probability of cold spells, and the question of reserve regulation in wintering canvasbacks. J Anim Ecol 63:11–23CrossRefGoogle Scholar
  27. Magurran AE (1999) The causes and consequences of geographic variation in antipredator behavior: perspectives from fish populations. In: Foster SA, Endler JA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, New York, pp 139–163Google Scholar
  28. McGowan A, Cresswell W, Ruxton GD (2002) The effects of daily weather variation on foraging and responsiveness to disturbance in overwintering Red Knot Calidris canutus. Ardea 90:229–237Google Scholar
  29. Myers JP (1981) A test of three hypotheses for latitudinal segregation of the sexes in wintering birds. Can J Zool 59:1527–1534Google Scholar
  30. Mysterud A (2000) The relationship between ecological segregation and sexual body size dimorphism in large herbivores. Oecologia 124:40–54CrossRefGoogle Scholar
  31. Nebel S (2005) Latitudinal clines in bill length and sex ratio in a migratory shorebird: a case of resource partitioning? Acta Oecol in press, doi:10.1016/j.actao.2005.02.002Google Scholar
  32. Nebel S, Latitudinal clines in sex ratio, bill and wing length in a migratory shorebird. J Field Ornithol in pressGoogle Scholar
  33. Nebel S, Thompson GJ (2005) Foraging behavior of Western Sandpipers changes with sediment temperature: implications for their hemispheric distribution. Ecol Res in press, doi:10.1007/s11284-005-0061-xGoogle Scholar
  34. Nebel S, Lank DB, O'Hara PD, Fernández G, Haase B, Delgado F, Estela FA, Evans Ogden LJ, Harrington B, Kus BE, Lyons JE, Mercier F, Ortego B, Takekawa JY, Warnock N, Warnock SE (2002) Western Sandpipers during the nonbreeding season: spatial segregation on a hemispheric scale. Auk 119:922–928CrossRefGoogle Scholar
  35. Nebel S, Cloutier A, Thompson GJ (2004) Molecular sexing of prey-remains permits a test of sex-biased predation in a wintering population of Western Sandpipers. Proc R Soc Lond B 271:S321–S323CrossRefGoogle Scholar
  36. Nolan V, Jr, Ketterson ED (1983) An analysis of body mass, wing length, and visible fat deposits of dark-eyed juncos wintering at different latitudes. Wilson Bull 95:603–620Google Scholar
  37. O'Hara PD (2002) The role of feather wear in alternative life history strategies of a long-distance migratory shorebird, the Western Sandpiper (Calidris mauri). PhD thesis. Simon Fraser University, BurnabyGoogle Scholar
  38. Page G, Fearis B (1971) Sexing Western Sandpipers by bill length. Bird Banding 42:297–298Google Scholar
  39. Piersma T, Hoekstra R, Dekinga A, Koolhaas A, Wolf P, Battley P, Wiersma P (1993) Scale and intensity of intertidal habitat use by knots Calidris canutus in the western Wadden Sea in relation to food, friends, and foes. Neth J Sea Res 31:331–357CrossRefGoogle Scholar
  40. Piersma T, Rogers DI, González PM, Zwarts L, Niles LJ, de Lima Serrano do Nascimento I, Minton CDT, Baker AJ (2005) Fuel storage rates in red knots worldwide: facing the severest ecological constraint in tropical intertidal conditions? In: Greenberg R, Marra PP (eds) Birds of two worlds: the ecology and evolution of migratory birds. Johns Hopkins University Press, Baltimore, pp 262–273Google Scholar
  41. Prater T, Marchant J, Vuorinen J (1977) Guide to the identification and ageing of Holarctic Waders, vol 17. British Trust for Ornithology, TringGoogle Scholar
  42. Reimchen TE (1980) Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can J Zool 58:1232–1244CrossRefGoogle Scholar
  43. Reimchen TE, Nosil P (2004) Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58:1274–1281PubMedGoogle Scholar
  44. Schmaljohann H, Dierschke V (2005) Optimal bird migration and predation risk: a field experiment with northern wheatears Oenanthe oenanthe. J Anim Ecol 74:131–138CrossRefGoogle Scholar
  45. Seghers BH (1973) An analysis of geographic variation in the antipredator adaptations of the guppy, Poecilia reticulata. PhD thesis. University of British Columbia, VancouverGoogle Scholar
  46. Shepherd PCF, Lank DB, Smith BD, Warnock N, Kaiser GW, Williams TD (2001) Sex ratios of Dunlin wintering at two latitudes on the Pacific coast. Condor 103:352–360CrossRefGoogle Scholar
  47. Suter W, van Eerden MR (1992) Simultaneous mass starvation of wintering diving ducks in Switzerland and The Netherlands: a wrong decision in the right strategy? Ardea 80:229–242Google Scholar
  48. Townshend DJ (1984) The effects of predators upon shorebird populations in the non-breeding season. Wader Study Group Bull 40:51–54Google Scholar
  49. Tulp I, Schekkerman H, Chylarecki P, Tomkovich P, Soloviev M, Bruinzeel L, van Dijk K, Hildén O, Hötker H, Kania W, van Roomen M, Sikora A, Summers R (2002) Body mass patterns of Little Stints at different latitudes during incubation and chick-rearing. Ibis 144:122–134CrossRefGoogle Scholar
  50. van der Veen IT, Linström KM (2000) Escape flights of yellowhammers and greenfinches: more than just physics. Anim Behav 59:593–601CrossRefPubMedGoogle Scholar
  51. Whitfield DP (2003) Redshank Tringa totanus flocking behavior, distance from cover and vulnerability to sparrowhawk Accipiter nisus predation. J Avian Biol 34:163–169CrossRefGoogle Scholar
  52. Wilson WH (1994) Western Sandpiper (Calidris mauri). In: Poole A, Gill F (eds) The birds of North America, vol 90. Academy of Natural Sciences, Philadelphia, Pennsylvania; American Ornithologists' Union, Washington, DCGoogle Scholar
  53. Witter MS, Cuthill IC, Bonser RHC (1994) Experimental investigations of mass-dependent predation risk in the European starling, Sturnus vulgaris. Anim Behav 48:201–222CrossRefGoogle Scholar
  54. Yasue M, Quinn JL, Cressell W (2003) Multiple effects of weather on the starvation and predation risk trade-off in choice of feeding location in Redshanks. Funct Ecol 17:727–736CrossRefGoogle Scholar
  55. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Stud Behav 16:229–249CrossRefGoogle Scholar
  56. Ydenberg RC, Butler RW, Lank DB, Guglielmo CG, Lemon M, Wolf N (2002) Trade-offs, condition dependence, and stopover site selection by migrating sandpipers. J Avian Biol 33:47–55CrossRefGoogle Scholar
  57. Ydenberg RC, Butler RW, Lank DB, Smith BD, Ireland J (2004) Western sandpipers have altered migration tactics as peregrine populations have recovered. Proc R Soc Lond B 271:1263–1269CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  2. 2.School of Biological, Earth & Environmental SciencesUniversity of New South WalesKensingtonAustralia

Personalised recommendations