Abstract
Annual migrations of birds profoundly influence terrestrial communities. However, few empirical studies examine why birds migrate, in part due to the difficulty of testing causal hypotheses in long-distance migration systems. Short-distance altitudinal migrations provide relatively tractable systems in which to test explanations for migration. Many past studies explain tropical altitudinal migration as a response to spatial and temporal variation in fruit availability. Yet this hypothesis fails to explain why some coexisting, closely-related frugivorous birds remain resident year-round. We take a mechanistic approach by proposing and evaluating two hypotheses (one based on competitive exclusion and the other based on differences in dietary specialization) to explain why some, but not all, tropical frugivores migrate. We tested predictions of these hypotheses by comparing diets, fruit preferences, and the relationships between diet and preference in closely-related pairs of migrant and resident species. Fecal samples and experimental choice trials revealed that sympatric migrants and residents differed in both their diets and fruit preferences. Migrants consumed a greater diversity of fruits and fewer arthropods than did their resident counterparts. Migrants also tended to have slightly stronger fruit preferences than residents. Most critically, diets of migrants more closely matched their preferences than did the diets of residents. These results suggest that migrants may be competitively superior foragers for fruit compared to residents (rather than vice versa), implying that current competitive interactions are unlikely to explain variation in migratory behavior among coexisting frugivores. We found some support for the dietary specialization hypothesis, propose refinements to the mechanism underlying this hypothesis, and discuss how dietary specialization might ultimately reflect past interspecific competition. We recommend that future studies quantify variation in nutritional content of tropical fruits, and determine whether frugivory is a consequence or a cause of migratory behaviour.
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References
Abrams PA (2006) The effects of switching behaviour on the evolutionary diversification of generalist consumers. Am Nat 168(5):645–659
Ackerly DD (2000) Taxon sampling, correlated evolution, and independent contrasts. Evolution 54(5):1480–1492
Alcock J (2005) Animal behaviour: an evolutionary approach. Sinauer Associates, Inc., Sunderland, MA
Alerstam T (1990) Bird Migration. Cambridge University Press, Cambridge, UK
Alerstam T, Hedenström A, Åkesson S (2003) Long-distance migration: evolution and determinants. Oikos 103(2):247–260
American Ornithologists’ Union (1998) Checklist of North American birds. American Ornithologists’ Union, Washington, DC
American Ornithologists’ Union (2005) Forty-sixth supplement to the American Ornithologists’ Union check-list of North American birds. Auk 122(3):1026–1031
Bell CP (2005) The origin and development of bird migration: comments on Rap Pole and Jones, and an alternative evolutionary model. Ardea 93(1):115–123
Bosque C, Calchi R (2003) Food choice by blue-gray tanagers in relation to protein content. Comp Biochem Physiol A 135(2):321–327
Bosque C, Pacheco A (2000) Dietary nitrogen as a limiting nutrient in frugivorous birds. Rev Chil Hist Nat 73(3):441–450
Boyle WA (2003) Seed images from the Atlantic slope of Costa Rica. http://eebwebarizonaedu/grads/alice/SeedPhotoshtml
Boyle WA (2006) Why do birds migrate? The role of food, habitat, predation, and competition. Ph.D., University of Arizona
Boyle WA (2008) Partial migration in birds: tests of three hypotheses in a tropical leaking frugivore. J Anim Ecol 77(6):1122–1128
Boyle WA (2009) How to keep tropical montane frugivorous birds in captivity. Ornitol Neotrop 20(2):265–273
Boyle WA (2010) Does food abundance explain altitudinal migration in a tropical frugivorous bird? Can J Zool-Rev Can Zool 88(2):204–213
Boyle WA, Conway CJ (2007) Why migrate? A test of the evolutionary precursor hypothesis. Am Nat 169(3):344–359
Bruderer B, Salewski V (2008) Evolution of bird migration in a biogeographical context. J Biogeogr 35(11):1951–1959
Burgess ND, Mlingwa COF (2000) Evidence for altitudinal migration of forest birds between montane Eastern Arc and lowland forests in East Africa. Ostrich 71(1–2):184–190
Carnicer J, Abrams PA, Jordano P (2008) Switching behavior, coexistence and diversification: comparing empirical community-wide evidence with theoretical predictions. Ecol Lett 11(8):802–808
Carnicer J, Jordano P, Melian CJ (2009) The temporal dynamics of resource use by frugivorous birds: a network approach. Ecology 90(7):1958–1970
Catry P, Campos A, Almada V et al (2004) Winter segregation of migrant European robins Erithacus rubecula in relation to sex, age and size. J Avian Biol 35(3):204–209
Chaves-Campos J (2004) Elevational movements of large frugivorous birds and temporal variation in abundance of fruits along an elevational gradient. Ornitol Neotrop 15(4):433–445
Chaves-Campos J, Arévalo JE, Araya M (2003) Altitudinal movements and conservation of Bare-necked Umbrellabird Cephalopteris glabricollis of the Tilarán Mountains, Costa Rica. Bird Conserv Intl 13(1):45–58
Connell JH (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35(2):131–138
Cox GW (1968) The role of competition in the evolution of migration. Evolution 22(1):180–192
Cristol DA, Baker MC, Corbone C (1999) Differential migration revisited: latitudinal segregation by age and sex class. Curr Ornith 15:33–88
del Hoyo J, Elliot A, Christie DA (eds) (1992–2009) Handbook of the birds of the world. Lynx Editions, Barcelona, Spain
Denslow JS, Levey DJ, Moermond TC et al (1987) A synthetic diet for fruit-eating birds. Wilson Bull 99(1):131–135
Dingle H (1996) Migration: the biology of life on the move. Oxford University Press, New York, NY
Elton CS (1973) The structure of invertebrate populations inside neotropical rain forest. J Anim Ecol 42:55–104
Fretwell SD (1980) Evolution of migration in relation to factors regulating bird numbers. In: Keast A, Morton ES (eds) Migrant birds in the neotropics. Smithsonian Institution Press, Washington, DC, pp 517–527
Greenberg R (1981) Dissimilar bill shapes in New World tropical versus temperate forest foliage-gleaning birds. Oecologia 49(2):143–147
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford, UK
Herrera CM (1998) Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-years study. Ecol Monogr 68(4):511–538
Herrera LG, Rodríguez GM, Hernández PP (2009) Sources of assimilated protein in a specialized tropical frugivorous bird, the yellow-throated Euphonia (Euphonia hirundinacea). Auk 126(1):175–180
Hobson KA, Wassenaar LI, Milá B et al (2003) Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia 136(2):302–308
Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54(3):687–708
Johnson DN, Maclean GL (1994) Altitudinal migration in Natal. Ostrich 65(2):86–94
Jordano P (1987) Frugivory, external morphology and digestive system in mediterranean sylviid warblers Sylvia spp. Ibis 129(2):175–189
Krebs CJ (2006) Ecology after 100 years: progress and pseudo-progress. NZ J Ecol 30(1):3–11
Levey DJ, Stiles FG (1992) Evolutionary precursors of long-distance migration: resource availability and movement patterns in Neotropical land birds. Am Nat 140(3):447–476
Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72(1):180–193
Magurran A (1988) Ecological diversity and its measurement. Chapman and Hall, London, UK
Martínez del Rio C, Restrepo C (1993) Ecological and behavioural consequences of digestion in frugivorous animals. Vegetatio 107(108):205–216
McPherson JM (1988) Preferences of cedar waxwings in the laboratory for fruit species, color and size: a comparison with field observations. Anim Behav 36:961–969
Oksanen L (1991) A century of community ecology: how much progress? Trends Ecol Evol 6(9):294–296
Pérez-Tris J, Tellería JL (2002) Migratory and sedentary blackcaps in sympatric non-breeding grounds: implications for the evolution of avian migration. J Anim Ecol 71(2):211–224
Raubenheimer D, Simpson SJ (1993) The geometry of compensatory feeding in the Locust. Anim Behav 45(5):953–964
Remsen JV, Jaramillo A, Nores M, et al. (2009) A classification of the bird species of South America. http://www.museum.lsu.edu/~Remsen/SACCBaseline.html
Rice WR, Gaines SD (1994) ‘Head I win, tails you lose’: testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol Evol 9(6):235–237
Rosselli L (1994) The annual cycle of the White-ruffed Manakin, Corapipo leucorrhoa, a tropical frugivorous altitudinal migrant, and its food plants. Bird Conserv Intl 4(2/3):143–160
Salewski V, Bruderer B (2007) The evolution of bird migration—a synthesis. Naturwissenschaften 94(4):268–279
Schaefer HM, Schmidt V, Bairlein F (2003) Discrimination abilities for nutrients: which difference matters for choosy birds and why? Anim Behav 65:531–541
Schluter D (2000) Ecological character displacement in adaptive radiation. Am Nat 156:S4–S16
Sherry TW (1984) Comparative dietary ecology of sympatric, insectivorous Neotropical flycatchers (Tyrannidae). Ecol Monogr 54(3):313–338
Sherry TW (1990) When are birds dietarily specialized? Distinguishing ecological from evolutionary approaches. Stud Avian Biol 13:337–352
Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New Haven, CT
Snow DW (1971) Evolutionary aspects of fruit-eating by birds. Ibis 113:194–202
Snow DW, Brooke MDL, Walther BA (2004) Family cotingidae (Cotingas). In: del Hoyo J, Elliot A, Christie DA (eds) Handbook of the birds of the world vol 9, Cotingus to Pipits and Wagtails. Lynx Editions, Barcelona, pp 32–109
Solórzano S, Castillo S, Valverde T et al (2000) Quetzal abundance in relation to fruit availability in a cloud forest of south-eastern Mexico. Biotropica 32(3):523–532
Stiles FG (1980) The annual cycle in a tropical wet forest hummingbird community. Ibis 122(3):322–343
Stiles FG (1983) Birds. In: Janzen DH (ed) Costa Rican natural history. University of Chicago Press, Chicago, IL, pp 502–530
Stiles FG, Skutch AF (1989) A field guide to the birds of costa rica. Cornell University Press, Ithaca, NY
Wheelwright NT (1983) Fruits and the ecology of resplendent quetzals. Auk 100(2):286–301
Wheelwright NT, Haber WA, Murray KG et al (1984) Tropical fruit-eating birds and their food plants: a survey of a Costa Rican lower montane forest. Biotropica 16(3):173–192
Whelan CJ, Willson MF (1994) Fruit choice in migrating North America birds: field and aviary experiments. Oikos 71:137–151
Whelan CJ, Schmidt KA, Steele BB et al (1998) Are bird-consumed fruits complementary resources? Oikos 83(1):195–205
Wiens JA (1989) The ecology of bird communities. Cambridge University Press, Cambridge, UK
Witmer MC (1998) Ecological and evolutionary implications of energy and protein requirements of avian frugivores eating sugary diets. Physiol Zool 71(6):599–610
Acknowledgments
H. Reider, R. Repasky L., Cholodenko, A. Zambrano, and J. Montoya-Morera, and provided exceptional field assistance. B. Boyle, B. Hammel, F. Morales, N. Zamora, C. Taylor, R. Kriebel, J. Gonzalez, and O. Vargas helped identify plants. Financial support was provided by the National Science Foundation (Grant No. 0410531), an NSERC (PGS-B) fellowship, the International Arid Lands Consortium, the American Ornithologists’ Union, and the University of Arizona. A. Bien, R. Tenorio, J. Guevara (MINAE permit #154-2002), and the University of Arizona IACUC (permit 02-068) provided permits and logistical support. R. Steidl, D. Levey, T. Fontaine, R. Greenberg and anonymous reviewers provided helpful comments on earlier versions of this manuscript.
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Boyle, W.A., Conway, C.J. & Bronstein, J.L. Why do some, but not all, tropical birds migrate? A comparative study of diet breadth and fruit preference. Evol Ecol 25, 219–236 (2011). https://doi.org/10.1007/s10682-010-9403-4
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DOI: https://doi.org/10.1007/s10682-010-9403-4