Life History Plasticity of a Tropical Seabird in Response to El Niño Anomalies during Early Life

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Ancona, Sergio ^a   Drummond, Hugh ^a  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; BREEDING; COHORT ANALYSIS; EL NINO; ENVIRONMENTAL TEMPERATURE; EVOLUTIONARY ADAPTATION; FEMALE; FLEDGLING; FOOD AVAILABILITY; HEAT; JUVENILE ANIMAL; LIFE HISTORY TRAIT; LONGEVITY; MALE; NONHUMAN; PERINATAL PERIOD; PRENATAL PERIOD; REPRODUCTIVE BEHAVIOR; SEABIRD; SEX DIFFERENCE; UNDERWEIGHT; WATER TEMPERATURE;

ANIMALS; BIRDS; BREEDING; EL NINO-SOUTHERN OSCILLATION; FEMALE; MALE; REPRODUCTION;

EID: 84883379543     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072665     Document Type: Article

References (86)

1. Lindström J, (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14: 343-348 doi: 10.1016/s0169-5347(99)01639-0.
2. Metcalfe NB, Monaghan P, (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16: 254-260 doi: 10.1016/s0169-5347(01)02124-3.
3. Cam E, Aubry L, (2011) Early development, recruitment and life history trajectory in long-lived birds. J Ornithol 152: 187-201 doi: 10.1007/s10336-011-0707-0.
4. Hector KL, Nakagawa S, (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol 81: 583-593 doi: 10.1111/j.1365-2656. 2011.019 42.x.
5. Hall AJ, McConnell BJ, Barker RJ, (2001) Factors affecting first-year survival in grey seals and their implications for life history strategy. J Anim Ecol 70: 138-149 doi: 10.1111/j.1365-2656.2001.00468.x.
6. Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P, (2003) Environmental variability, life-history covariation and cohort effects in the red-billed chough Pyrrhocorax pyrrhocorax. J Anim Ecol 72: 36-46 doi: 10.1046/j.1365-2656.2003.00673.x.
7. Braasch A, Schauroth C, Becker P, (2009) Post-fledging body mass as a determinant of subadult survival in common terns Sterna hirundo. J Ornithol 150: 401-407 doi: 10.1007/s10336-008-0362-2.
8. Albon SD, Clutton-Brock TH, Guinness FE, (1987) Early development and population dynamics in red deer. II. Density-independent effects and cohort variation. J Anim Ecol 56: 69-81 doi: 10.2307/4800.
9. Cam E, Monnat JY, Hines JE, (2003) Long-term fitness consequences of early conditions in the kittiwake. J Anim Ecol 72: 411-424 doi: 10.1046/j.1365-2656.2003.00708.x.
10. Wilkin TA, Sheldon BC, (2009) Sex differences in the persistence of natal environmental effects on life histories. Curr Biol 19: 1998-2002 doi: 10.1016/j.cub.2009.09.065.
11. Drummond H, Torres R, Krishnan VV, (2003) Buffered development: resilience after aggressive subordination in infancy. Am Nat 161: 794-807 doi: 10.1086/375170.
12. Nussey DH, Kruuk LEB, Morris A, Clutton-Brock TH, (2007) Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr Biol 17: R1000-R1001 doi: 10.1016/j.cub.2007.10.005.
13. Kruuk LEB, Clutton-Brock TH, Rose KE, Guinness FE, (1999) Early determinants of lifetime reproductive success differ between the sexes in red deer. Proc R Soc Biol Sci Ser B 266: 1655-1661 doi: 10.1098/rspb.1999.0828.
14. Metcalfe NB, Monaghan P, (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38: 935-940 doi: 10.1016/s0531-5565(03)00159-1.
15. Reed ET, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, et al. (2008) Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. Am Nat 171: E89-E101 doi: 10.1086/524957.
16. Moyes K, Morgan BJT, Morris A, Morris SJ, Clutton-Brock TH, et al. (2009) Exploring individual quality in a wild population of red deer. J Anim Ecol 78: 406-413 doi: 10.1111/j.1365-2656.2008.01497.x.
17. Sedinger JS, Flint PL, Lindberg MS, (1995) Environmental influence on life-history traits: growth, survival, and fecundity in black brant (Branta bernicla). Ecology 76: 2404-2414 doi: 10.2307/2265816.
18. Descamps S, Boutin S, Berteaux D, Gaillard JM, (2008) Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117: 1406-1416 doi: 10.1111/j.0030-1299.2008.16545.x.
19. Jones KS, Nakagawa S, Sheldon BC, (2009) Environmental sensitivity in relation to size and sex in birds: Meta-regression analysis. Am Nat 174: 122-133 doi: 10.1086/599299.
20. Mora JO, Sánchez R, De Paredes B, Herrera MG, (1981) Sex related effects of nutritional supplementation during pregnancy on fetal growth. Early Hum Dev 5: 243-251 doi: 10.1016/0378-3782(81)90032-3.
21. Nager RG, Monaghan P, Griffiths R, Houston DC, Dawson R, (1999) Experimental demonstration that offspring sex ratio varies with maternal condition. Proc Natl Acad Sci USA 96: 570-573 doi: 10.1073/pnas.96.2.570.
22. Gorman HE, Nager RG, (2004) Prenatal developmental conditions have long-term effects on offspring fecundity. Proc R Soc Biol Sci Ser B 271: 1923-1928 doi: 10.1098/rspb.2004.2799.
23. Solberg EJ, Loison A, Gaillard JM, Heim M, (2004) Lasting effects of conditions at birth on moose body mass. Ecography 27: 677-687 doi: 10.1111/j.0906-7590.2004.03864.x.
24. Cox RM, Calsbeek R, (2009) Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am Nat 173: 176-187 doi: 10.1086/595841.
25. Mousseau TA, Fox CW, (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13: 403-407 doi: 10.1016/s0169-5347(98)01472-4.
26. Monaghan P, (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans R Soc Biol Sci Ser B 363: 1635-1645 doi: 10.1098/rstb.2007.0011.
27. Naguib M, Nemitz A, Gil D, (2006) Maternal developmental stress reduces reproductive success of female offspring in zebra finches. Proc R Soc Biol Sci Ser B 273: 1901-1905 doi: 10.1098/rspb.2006.3526.
28. Van de Pol M, Bruinzeel LW, Heg DIK, Van der Jeugd HP, Verhulst S, (2006) A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). J Anim Ecol 75: 616-626 doi: 10.1111/j.1365-2656.2006.01079.x.
29. Taborsky B, (2006) The influence of juvenile and adult environments on life-history trajectories. Proc R Soc Biol Sci Ser B 273: 741-750 doi: 10.1098/rspb.2005.3347.
30. Lummaa V, Clutton-Brock TH, (2002) Early development, survival and reproduction in humans. Trends Ecol Evol 17: 141-147 doi: 10.1016/S0169-5347(01)02414-4.
31. Skinner MK, Manikkam M, Guerrero-Bosagna C, (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21: 214-222 doi: 10.1016/j.tem.2009.12.007.
32. Gluckman PD, Hanson MA, Beedle AS, (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol 19: 1-19 doi: 10.1002/ajhb.20590.
33. Blount JD, Metcalfe NB, Arnold KE, Surai PF, Devevey GL, et al. (2003) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc R Soc Biol Sci Ser B 270: 1691-1696 doi: 10.1098/rspb.2003.2411.
34. Royle NJ, Lindström J, Metcalfe NB, (2005) A poor start in life negatively affects dominance status in adulthood independent of body size in green swordtails Xiphophorus helleri. Proc R Soc Biol Sci Ser B 272: 1917-1922 doi: 10.1098/rspb.2005.3190.
35. Roff DA (2002) Life history evolution. Massachusetts: Sinauer Associates. 527 p.
36. Auer SK, (2010) Phenotypic plasticity in adult life-history strategies compensates for a poor start in life in trinidadian guppies (Poecilia reticulata). Am Nat 176: 818-829 doi: 10.1086/657061.
37. Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC, (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. J Evol Biol 22: 387-395 doi: 10.1111/j.1420-9101.2008.01656.x.
38. de Kogel CH, (1997) Long-term effects of brood size manipulation on morphological development and sex-specific mortality of offspring. J Anim Ecol 66: 167-178 doi: 10.2307/6019.
39. Erikstad KE, Fauchald P, Tveraa T, Steen H, (1998) On the cost of reproduction in long-lived birds: the influence of environmental variability. Ecology 79: 1781-1788 doi: [];10.1890/0012-9658(1998)079[1781:otcori]2.0.co;2.
40. Greig SA, Coulson JC, Monaghan P, (1983) Age-related differences in foraging success in the herring gull (Larus argentatus). Anim Behav 31: 1237-1243 doi: 10.1016/s0003-3472(83)80030-x.
41. Bruinzeel LW, Van de Pol M, (2004) Site attachment of floaters predicts success in territory acquisition. Behav Ecol 15: 290-296 doi: 10.1093/beheco/arh019.
42. Lewis S, Nussey DH, Wood AG, Croxall JP, Phillips RA, (2012) Intrinsic determinants of a population trend in timing of breeding in the wandering albatross. Oikos 000: 001-011 doi: 10.1111/j.1600-0706.2012.20293.x.
43. Lewis S, Elston DA, Daunt F, Cheney B, Thompson PM, (2009) Effects of extrinsic and intrinsic factors on breeding success in a long lived seabird. Oikos 118: 521-528 doi: 10.1111/j.1600-0706.2009.17308.x.
44. Stenseth NC, Mysterud A, Ottersen G, Hurrell JW, Chan KS, et al. (2002) Ecological effects of climate fluctuations. Science 297: 1292-1296 doi: 10.1126/science.1071281.
45. Helmuth B, Kingsolver JG, Carrington E, (2005) Biophysics, physiological ecology, and climate change: Does mechanism matter? Annu Rev Physiol 67: 177-201 doi: 10.1146/annurev.physiol.67.040403.105027.
46. Post E, Stenseth NC, (1999) Climatic variability, plant phenology, and northern ungulates. Ecology 80: 1322-1339 doi: [];10.1890/00129658(1999)080[1322:cvppan]2.0. co;2).
47. Sæther BE, Tufto J, Engen S, Jerstad K, Røstad OW, et al. (2000) Population dynamical consequences of climate change for a small temperate songbird. Science 287: 854-856 doi: 10.1126/science.287.5454.854.
48. Devney CA, Caley MJ, Congdon BC, (2010) Plasticity of noddy parents and offspring to sea-surface temperature anomalies. PLoS ONE 5: e11891 doi: 10.1371/journal.pone.0011891.
49. Lindström J, Kokko H, (2002) Cohort effects and population dynamics. Ecol Lett 5: 338-344 doi: 10.1046/j.1461-0248.2002.00317.x.
50. Post E, Stenseth NC, Langvatn R, Fromentin JM, (1997) Global climate change and phenotypic variation among red deer cohorts. Proc R Soc Biol Sci Ser B 264: 1317-1324 doi: 10.1098/rspb.1997.0182.
51. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. Chicago: The University of Chicago Press. 378 p.
52. Forchhammer MC, Clutton-Brock TH, Lindström J, Albon SD, (2001) Climate and population density induce long-term cohort variation in a northern ungulate. J Anim Ecol 70: 721-729 doi: 10.1046/j.0021-8790.2001.00532.x.
53. Thompson PM, Ollason JC, (2001) Lagged effects of ocean climate change on fulmar population dynamics. Nature 413: 417-420 doi: 10.1038/35096558.
54. Nevoux M, Weimerskirch H, Barbraud C, (2010) Long- and short-term influence of environment on recruitment in a species with highly delayed maturity. Oecologia 162: 383-392 doi: 10.1007/s00442-009-1482-y.
55. Nelson JB (2006) Pelicans, cormorants and their relatives: The Pelecaniformes. Oxford: Oxford University Press. 680 p.
56. Oro D, Torres R, Rodríguez C, Drummond H, (2010) Climatic influence on demographic parameters of a tropical seabird varies with age and sex. Ecology 91: 1205-1214 doi: 10.1890/09-0939.1.
57. Ancona S, Sánchez-Colón S, Rodríguez C, Drummond H, (2011) El Niño in the warm tropics: local sea temperature predicts breeding parameters and growth of blue-footed boobies. J Anim Ecol 80: 799-808 doi: 10.1111/j.13652656.2011.01821.x.
58. Ancona S, Calixto-Albarrán I, Drummond H, (2012) Effect of El Niño on the diet of a specialist seabird, Sula nebouxii, in the warm eastern tropical Pacific. Mar Ecol Prog Ser 462: 261-271 doi: 10.3354/meps09851.
59. Anderson DJ, Ricklefs RE, (1987) Radio-tracking masked and blue-footed boobies (Sula spp.) in the Galápagos Islands. Natl Geo Res 3: 152-163.
60. Guerra M, Drummond H, (1995) Reversed sexual size dimorphism and parental care: minimal division of labour in the blue-footed booby. Behaviour 132: 479-496 doi: 10.1163/156853995x00162).
61. Torres R, Drummond H, (1997) Female-biased mortality in nestlings of a bird with size dimorphism. J Anim Ecol 66: 859-865 doi: 10.2307/6001.
62. Torres R, Drummond H, (1999) Variably male-biased sex ratio in a marine bird with females larger than males. Oecologia 118: 16-22 doi: 10.1007/s004420050698.
63. Torres R, Drummond H (2009) Variably male-biased sex ratio in a marine bird with females larger than males. Oecologia 161: 447-448. [Erratum to Oecologia 118: 16-22]. doi: 10.1007/s00442-009-1378-x.
64. Osorio-Beristain M, Drummond H, (1993) Natal dispersal and deferred breeding in the blue-footed booby. Auk 110: 234-239.
65. Velando A, Drummond H, Torres R, (2006) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc R Soc Biol Sci Ser B 273: 1443-1448 doi: 10.1098/rspb.2006.3480.
66. Beamonte-Barrientos R, Velando A, Drummond H, Torres R, (2010) Senescence of maternal effects: aging influences egg quality and rearing capacities of a long-lived bird. Am Nat 175: 469-480 doi: 10.1086/650726.
67. Kim SY, Velando A, Torres R, Drummond H, (2011) Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird. Oecologia 166: 615-626 doi: 10.1007/s00442-011-1914-3.
68. Velando A, Drummond H, Torres R, (2010) Senescing sexual ornaments recover after a sabbatical. Biol Lett 6: 194-196 doi: 10.1098/rsbl.2009.0759.
69. Peña B (2009) Variación de la fecha de puesta del bobo de patas azules. B.Sc. Thesis. Universidad Nacional Autónoma de México.
70. Frankignoul C, (1985) Sea surface temperature anomalies, planetary waves, and air-sea feedback in the middle latitudes. Rev Geophys 23: 357-390 doi: 10.1029/RG023i004p00357.
71. Böhning D, Dietz E, Schlattmann P, Mendoca L, Kirchner U, (1999) The zero-inflated Poisson model and the decayed, missing and filled teeth index in dental epidemiology. J R Statist Soc Ser A 162: 195-209.
72. Crawley MJ (2007) The R Book. West Sussex: John Wiley & Sons Ltd. 950 p.
73. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
74. Weimerskirch H, (1992) Reproductive effort in long-lived birds: age-specific patterns of condition, reproduction and survival in the wandering albatross. Oikos 64: 464-473 doi: 10.2307/3545162.
75. Morrison KW, Hipfner JM, Gjerdrum C, Green DJ, (2009) Wing length and mass at fledging predict local juvenile survival and age at first return in tufted puffins. Condor 111: 433-441 doi: 10.1525/cond.2009.080099.
76. Stienen EWM, Brenninkmeijer A, (2002) Variation in growth in sandwich tern chicks Sterna sandvicensis and the consequences for pre- and post-fledging mortality. Ibis 144: 567-576 doi: 10.1046/j.1474-919X.2002.00086.x.
77. Moe B, Brunvoll S, Mork D, Brobakk TE, Bech C, (2004) Developmental plasticity of physiology and morphology in diet-restricted European shag nestlings (Phalacrocorax aristotelis). J Exp Biol 207: 4067-4076 doi: 10.1242/jeb.01226.
78. Bateson P, Barker D, Clutton-Brock TH, Deb D, D'Udine B, et al. (2004) Developmental plasticity and human health. Nature 430: 419-421 doi: 10.1038/nature02725.
79. Torres R, Drummond H, (1999) Does large size make daughters of the blue-footed booby more expensive than sons? J Anim Ecol 68: 1133-1141 doi: 10.1046/j.1365-2656.1999.00357.x.
80. Weimerskirch H, Shaffer SA, Tremblay Y, Costa DP, Gadenne H, et al. (2009) Species- and sex-specific differences in foraging behaviour and foraging zones in blue-footed and brown boobies in the Gulf of California. Mar Ecol Prog Ser 391: 267-278 doi: 10.3354/meps07981.
81. Dentressangle F, Boeck L, Torres R, (2008) Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol 62: 1899-1908 doi: 10.1007/s00265-008-0620-6.
82. Young RL, Badyaev AV, (2004) Evolution of sex-biased maternal effects in birds: I. Sex-specific resource allocation among simultaneously growing oocytes. J Evol Biol 17: 1355-1366 doi: 10.1111/j.1420-9101.2004.00762.x.
83. Deeming DC, Ferguson MWJ (1991) Egg incubation: Its effects on embryonic development in birds and reptiles. Cambridge: Cambridge University Press. 448 p.
84. Schwabl H, Mock DW, Gieg JA, (1997) A hormonal mechanism for parental favouritism. Nature 386: 231-231 doi: 10.1038/386231a0.
85. Trivers RL, Willard DE, (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90-92 doi: 10.1126/science.179.4068.90.
86. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, et al. (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14: 159-166 doi: 10.1038/sj.ejhg.5201538.