Telomere length and environmental conditions predict stress levels but not parental investment in a long-lived seabird

Marine Ecology Progress Series

Volumn 556, Issue , 2016, Pages 251-259

  Young, Rebecca C ^a,c   Barger, Chris P ^a,d   Dorresteijn, Ine ^a,e   Haussmann, Mark F ^b   Kitaysky, Alexander S ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b BUCKNELL UNIVERSITY   (United States)

^c Bucknell University ^*  (United States)

^d ALASKA DEPARTMENT OF FISH AND GAME   (United States)

^e LEUPHANA UNIVERSITY OF LÜNEBURG   (Germany)

Author keywords

Br nnich's guillemot; Corticosterone; Individual quality; Parental investment; Telomeres; Temperature depth recorder; Thick billed murre; Uria lomvia

Indexed keywords

BIOMARKER; BODY CONDITION; CHROMOSOME; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; HORMONE; PARENTAL INVESTMENT; PHYSIOLOGICAL RESPONSE; PREDICTION; REPRODUCTION; SEABIRD; TEMPERATURE EFFECT; BREEDING; PARENTAL CARE;

BERING SEA; PACIFIC OCEAN;

AVES; URIA LOMVIA;

EID: 84989163822     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps11864     Document Type: Article

References (61)

1. Aydinonat D, Penn DJ, Smith S, Moodley Y, Hoelzl F, Knauer F, Schwarzenberger F (2014) Social isolation shortens telomeres in African grey parrots (Psittacus erithacus erithacus). PLOS ONE 9: e93839
2. Barger CP, Kitaysky AS (2012) Isotopic segregation between sympatric seabird species increases with nutritional stress. Biol Lett 8: 442-445
3. Barrett ELB, Burke TA, Hammers M, Komdeur J, Richardson DS (2013) Telomere length and dynamics predict mortality in a wild longitudinal study. Mol Ecol 22: 249-259
4. Barrett RT, Erikstad KE, Sandvik H, Myksvoll M and others (2015) The stress hormone corticosterone in a marine top predator reflects short-term changes in food availability. Ecol Evol 5: 1306-1317
5. Beirne C, Delahay R, Hares M, Young A (2014) Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal. PLOS ONE 9: e108964
6. Benowitz-Fredericks ZM, Shultz MT, Kitaysky AS (2008) Stress hormones suggest opposite trends of food availability for planktivorous and piscivorous seabirds in 2 years. Deep-Sea Res II 55: 1868-1876
7. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proc R Soc Lond Biol Sci 276: 1679-1683
8. Boldina I, Beninger PG (2016) Strengthening statistical usage in marine ecology: linear regression. J Exp Mar Biol Ecol 474: 81-91
9. Bryant R, Jones IL, Hipfner JM (1999) Responses to changes in prey availability by common murres and thick-billed murres at the Gannet Islands, Labrador. Can J Zool 77: 1278-1287
10. Burger AE, Piatt JF (1990) Flexible time budgets in breeding common murres: buffers against variable prey abundance. Stud Avian Biol 14: 71-83
11. Buxton J, Walters RG, Das S, Lagou V and others (2012) Genetic and environmental influences on leukocyte telomere length: studies in Northern Finns reveal gender differences. J Med Genet 49: S23
12. Byrd GV, Schmutz JA, Renner HM (2008) Contrasting population trends of piscivorous seabirds in the Pribilof Islands: a 30-year perspective. Deep-Sea Res II 55: 1846-1855
13. Catry P, Poisbleau M, Lecoq M, Phillips RA (2013) Differences in the timing and extent of annual moult of blackbrowed albatrosses Thalassarche melanophris living in contrasting environments. Polar Biol 36: 837-842
14. de Forest LN, Gaston AJ (1996) The effect of age on timing of breeding and reproductive success in the thick-billed murre. Ecology 77: 1501-1511
15. Dorresteijn I, Kitaysky AS, Barger C, Benowitz-Fredericks ZM, Byrd GV, Schultz M, Young R (2012) Climate affects food availability to planktivorous least auklets Aethia pusilla through physical processes in the southeastern Bering Sea. Mar Ecol Prog Ser 454: 207-220
16. Elliott KH, Gaston AJ, O'Reilly KM, Speakman JR, Davoren GK (2014) The prudent parent meets old age: a high stress response in very old seabirds supports the terminal restraint hypothesis. Horm Behav 66: 828-837
17. Elliott KH, Hare JF, Gaston AJ, Ropert-Coudert Y, Anderson WG (2015) Ageing gracefully: physiology but not behaviour declines with age in diving birds. Funct Ecol 29: 219-228
18. Gaston AJ, Hipfner JM (2006) Adult Brünnich's guillemots Uria lomvia balance body condition and investment in chick growth. Ibis 148: 106-113
19. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075
20. Gruber H, Schaible R, Ridgway ID, Chow TT, Held C, Philipp EER (2014) Telomere-independent ageing in the longest-lived non-colonial animal, Arctica islandica. Exp Gerontol 51: 38-45
21. Hall ME, Nasir L, Daunt F, Gault EA, Croxall JP, Wanless S, Monaghan P (2004) Telomere loss in relation to age and early environment in long-lived birds. Proc R Soc Lond B Biol Sci 271: 1571-1576
22. Harding AMA, Paredes R, Suryan R, Roby D and others (2013) Does location really matter? An inter-colony comparison of seabirds breeding at varying distances from productive oceanographic features in the Bering Sea. Deep-Sea Res II 94: 178-191
23. Hare SR, Mantua NJ (2000) Empirical evidence for North Pacific regime shifts in 1977 and 1989. Prog Oceanogr 47: 103-145
24. Hatakeyama H, Nakamura KI, Izumiyama-Shimomura N, Ishii A, Tsuchida S, Takubo K, Ishikawa N (2008) The teleost Oryzias latipes shows telomere shortening with age despite considerable telomerase activity throughout life. Mech Ageing Dev 129: 550-557
25. Haussmann MF, Marchetto NM (2010) Telomeres: linking stress and survival, ecology and evolution. Curr Zool 56: 714-727
26. Haussmann MF, Mauck RA (2008a) New strategies for telomere-based age estimation. Mol Ecol Resour 8: 264-274
27. Haussmann MF, Mauck RA (2008b) Telomeres and longevity: testing an evolutionary hypothesis. Mol Biol Evol 25: 220-228
28. Haussmann MF, Winkler DW, O'Reilly KM, Huntington CE, Nisbet ICT, Vleck CM (2003) Telomeres shorten more slowly in long-lived birds and mammals than in shortlived ones. Proc R Soc Lond B Biol 270: 1387-1392
29. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P (2012) Telomere length in early life predicts lifespan. Proc Natl Acad Sci USA 109: 1743-1748
30. Hemann MT, Strong MA, Hao LY, Greider CW (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107: 67-77
31. Herborn KA, Heidinger BJ, Boner W, Noguera JC, Adam A, Daunt F, Monaghan P (2014) Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc R Soc Lond B Biol Sci 281: 20133151
32. Ito M, Takahashi A, Kokubun N, Kitaysky AS, Watanuki Y (2010) Foraging behavior of incubating and chick-rearing thick-billed murres Uria lomvia. Aquat Biol 8: 279-287
33. Kitaysky AS, Hunt GL Jr, Flint EN, Rubega MA, Decker MB (2000) Resource allocation in breeding seabirds: re-sponses to fluctuations in their food supply. Mar Ecol Prog Ser 206: 283-296
34. Kitaysky AS, Piatt JF, Hatch SA, Kitaiskaia EV, Benowitz-Fredericks ZM, Shultz MT, Wingfield JC (2010) Food availability and population processes: severity of nutritional stress during reproduction affects persistence of seabirds in a colony. Funct Ecol 24: 625-637
35. Laaksonen T, Korpimaki E, Hakkarainen H (2002) Interactive effects of parental age and environmental variation on the breeding performance of Tengmalm's owls. J Anim Ecol 71: 23-31
36. Le Vaillant M, Viblanc V, Saraux C, Le Bohec C and others (2015) Telomere length reflects individual quality in free-living adult king penguins. Polar Biol 38: 2059-2067
37. Lewis S, Wanless S, Elston DA, Schultz M and others (2006) Determinants of quality in a long-lived colonial species. J Anim Ecol 75: 1304-1312
38. Mizutani Y, Tomita N, Niizuma Y, Yoda K (2013) Environmental perturbations influence telomere dynamics in longlived birds in their natural habitat. Biol Lett 9: 20130511
39. Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21: 47-53
40. Müezzinler A, Zeineddine AK, Brenner H (2013) A systematic review of leukocyte telomere length and age in adults. Ageing Res Rev 12: 509-519
41. Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz TS, Blomqvist D (2011) Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLOS ONE 6: e17473
42. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118: 1883-1891
43. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.r-project.org
44. Reed TE, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, Harris MP (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
45. Riechert J, Becker PH, Chastel O (2014) Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance. Oecologia 176: 715-727
46. Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol Part A Mol Integr Physiol 140: 73-79
47. Salomons HM, Mulder GA, van de Zande L, Haussmann MF, Linskens MHK, Verhulst S (2009) Telomere shortening and survival in free-living corvids. Proc R Soc Lond B Biol Sci 276: 3157-3165
48. Satterthwaite W, Kitaysky AS, Mangel M (2012) Linking climate variability, productivity and stress to demography in a long-lived seabird. Mar Ecol Prog Ser 454: 221-235
49. Schultner J, Kitaysky AS, Welcker J, Hatch SA (2013) Fat or lean: adjustment of endogenous energy stores to predictable and unpredictable changes in allostatic load. Funct Ecol 27: 45-55
50. Schultner J, Moe B, Chastel O, Bech C, Kitaysky AS (2014) Migration and stress during reproduction govern telomere dynamics in a seabird. Biol Lett 10: 20130889
51. Shalev I (2012) Early life stress and telomere length: investigating the connection and possible mechanisms. BioEssays 34: 943-952
52. Smith DL Jr, Mattison JA, Desmond RA, Gardner JP and others (2011) Telomere dynamics in rhesus monkeys: no apparent effect of caloric restriction. J Gerontol A Biol Sci Med Sci 66: 1163-1168
53. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioral ecology using Akaike's information criterion. Behav Ecol Sociobiol 65: 13-21
54. Thaxter CB, Daunt F, Hamer KC, Watanuki Y and others (2009) Sex-specific food provisioning in a monomorphic seabird, the common guillemot Uria aalge: nest defence, foraging efficiency or parental effort? J Avian Biol 40: 75-84
55. Tigano A, Damus M, Birt TP, Morris-Pocock JA, Artukhin Y, Friesen VL (2015) The Arctic: glacial refugium or area of secondary contact? Inference from the population genetic structure of the thick-billed murre (Uria lomvia), with implications for management. J Hered 106: 238-246
56. Wiebe KL, Martin K (1998) Age-specific patterns of reproduction in white-tailed and willow ptarmigan Lagopus leucurus and L. lagopus. Ibis 140: 14-24
57. Wingfield JC, Farner DS (1975) The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding. Steroids 26: 311-327
58. Wingfield JC, Hegner RE, Lewis DM (1991) Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding whitebrowed sparrow weaver, Plocepasser mahali. J Zool 225: 43-58
59. Young RC, Kitaysky AS, Haussmann MF, Descamps S, Orben R, Elliott KH, Gaston AJ (2013) Age, sex, and telomere dynamics in a long-lived seabird with male-biased parental care. PLOS ONE 8: e74931
60. Young RC, Kitaysky AS, Barger CP, Dorresteijn I, Ito M, Watanuki Y (2015) Telomere length is a strong predictor of foraging behavior in a long-lived seabird. Ecosphere 6: art39
61. Zou Y, Sfeir A, Gryaznov SM, Shay JW, Wright WE (2004) Does a sentinel or a subset of short telomeres determine replicative senescence? Mol Biol Cell 15: 3709-3718