Environmental and Physiological Influences to Isotopic Ratios of N and Protein Status in a Montane Ungulate in Winter

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Gustine, David D ^a   Barboza, Perry S ^b   Adams, Layne G ^a   Wolf, Nathan B ^c  

^a Alaska Biological Science Center   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^c UNIVERSITY OF ALASKA ANCHORAGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; NITROGEN; NITROGEN 15; PROTEIN; PROTEIN INTAKE; SNOW;

ADULT; AMINO ACID BLOOD LEVEL; ARTICLE; DIET RESTRICTION; ENVIRONMENTAL FACTOR; ERYTHROCYTE; FEMALE; NATIONAL PARK; NONHUMAN; POPULATION DENSITY; POPULATION SIZE; REINDEER; UNGULATE; UNITED STATES; WINTER; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL FOOD; BLOOD; BODY COMPOSITION; CHEMISTRY; COLD; METABOLISM; PHYSIOLOGY; POPULATION DYNAMICS; PROTEIN INTAKE; REGRESSION ANALYSIS; REPRODUCTION; SEASON;

ALASKA; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BODY COMPOSITION; COLD TEMPERATURE; DIETARY PROTEINS; FEMALE; NITROGEN; POPULATION DENSITY; POPULATION DYNAMICS; REGRESSION ANALYSIS; REINDEER; REPRODUCTION; SEASONS; SNOW;

EID: 84905454593     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103471     Document Type: Article

References (79)

1. Clutton-Brock TH (1982) Red deer: behavior and ecology of two sexes. Chicago, IL: The University of Chicago Press.
2. Helle T, Kojola I (2008) Demographics in an alpine reindeer herd: effects of density and winter weather. Ecography 31: 221-230. (Pubitemid 351457530)
3. Tyler NC, Forchhammer MC, Oritsland NA (2008) Nonlinear effects of climate and density in the dynamics of a fluctuating population of reindeer. Ecology 89: 1675-1686.
4. Albon SD, Cluttonbrock TH, Guinness FE (1987) Early development and population dynamics in red deer. II. Density-independent effects and cohort variation. Journal of Animal Ecology 56: 69-81.
5. Forchhammer MC, Post E, Stenseth NC, Boertmann DM (2002) Long-term responses in arctic ungulate dynamics to changes in climatic and trophic processes. Population Ecology 44: 113-120. (Pubitemid 35169533)
6. Adams LG (2003) Marrow fat deposition and skeletal growth in caribou calves. Journal of Wildlife Management 67: 20-24.
7. Adams LG (2005) Effects of maternal characteristics and climatic variation on birth masses of Alaskan caribou. Journal of Mammalogy 86: 506-513.
8. Bårdsen BJ, Henden J, Fauchald P, Tveraa T, Stien A (2011) Plastic reproductive allocation as a buffer against environmental stochaticity - linking life history and population dynamics to climate. Oikos 120: 245-257.
9. Cote SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127: 230-238. (Pubitemid 32449376)
10. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68: 225-252.
11. Stephens PA, Houston AI, Harding KC, Boyd IL, McNamara JM (2013) Capital and income breeding: the role of food supply. Ecology 95: 882-896.
12. Andersen R, Gaillard J-M, Linnell JDC, Duncan P (2000) Factors affecting maternal care in an income breeder, the European roe deer. Journal of Animal Ecology 69: 672-682. (Pubitemid 30597761)
13. White RG (1983) Foraging patterns and their multiplier effects on productivity of northern ungulates. Oikos 40: 377-384.
14. Clutton-Brock TH (1991) The evolution of parental care. Princeton, New Jersey: Princeton University Press. 352 p.
15. Martin JGA, Festa-Bianchet M (2010) Bighorn ewes transfer the costs of reproduction to their lambs. The American Naturalist 176: 414-423.
16. White RG, Luick JR (1984) Plasticity and constraints in the lactational strategy of reindeer and caribou. Symposium of the Zoological Society of London 51: 215-232.
17. Festa-Bianchet M, Jorgenson JT (1998) Selfish mothers: Reproductive expenditure and resource availability in bighorn ewes. Behavioral Ecology 9: 144-150. (Pubitemid 28159432)
18. Gustine DD, Barboza PS, Lawler JP (2010) Dynamics of body protein and the implications for reproduction in captive muskoxen (Ovibos moschatus) during winter. Physiological and Biochemical Zoology 83: 687-697.
19. Hamel S, Côté S (2009) Foraging decisions in a capital breeder: trade-offs between mass gain and lactation. Oecologia 161: 421-432.
20. Hamel S, Côté SD, Festa-Bianchet M (2010) Maternal characteristics and environment affect the costs of reproduction in female mountain goats. Ecology 91: 2034-2043.
21. Barboza PS, Parker KL (2008) Allocating protein to reproduction in Arctic reindeer and caribou. Physiological and Biochemical Zoology 81: 835-855.
22. Taillon J, Barboza PS, Côté SD (2013) Nitrogen allocation to offspring and milk production in a capital breeder. Ecology 94: 1815-1827.
23. Lesage L, Crete M, Huot J, Ouellet JP (2001) Evidence for a trade-off between growth and body reserves in northern white-tailed deer. Oecologia 126: 30-41. (Pubitemid 32442509)
24. Robbins CT, Podbielancik-Norman RS, Wilson DL, Mould ED (1981) Growth and nutrient consumption of elk calves compared to other ungulate species. Journal of Wildlife Management 45: 172-186.
25. Parker KL, Barboza PS, Gillingham MP (2009) Nutrition integrates environmental responses of ungulates. Functional Ecology 23: 57-69.
26. Oftedal OT (1985) Pregnancy and lactation. In: R. J Hudson and R. G White, editors. Bioenergetics of Wild Herbivores. Boca Raton, FL: CRC Press, Inc. pp. 216-238.
27. Chan-McLeod AC, White RG, Holleman DF (1994) Effects of protein and energy intake, body condition, and season on nutrient partitioning and milk production in caribou and reindeer. Canadian Journal of Zoology 72: 938-947. (Pubitemid 2140845)
28. Landete-Castillejos T, Garcia AJ, Gallego L (2001) Calf growth in captive Iberian red deer (Cervus elaphus hispanicus): effects of birth date and hind milk production and composition. Journal of Animal Science 79: 1085-1092. (Pubitemid 33609521)
29. Barboza PS, Parker KL (2006) Body protein stores and isotopic indicators of N balance in female reindeer (Rangifer tarandus) during winter. Physiological and Biochemical Zoology 79: 628-644. (Pubitemid 43846277)
30. Karasov WH, Martinez del Rio C (2007) Chapter 8: Isotopic ecology. Physiological ecology: how animals process energy, nutrients, and toxins. Princeton, NJ: Princeton University Press. pp. 741.
31. Barboza PS, Parker KL, Hume ID (2009) Integrative Wildlife Nutrition. Berlin, Heidelberg Germany: Springer-Verlag.
32. Finstad GL, Kielland K (2011) Landscape variation in the diet and productivity of reindeer in Alaska based on stable isotope analyses. Arctic Antarctic and Alpine Research 43: 543-554.
33. Taillon J, Barboza PS, Cote SD (2013) Nitrogen allocation to offspring and milk production in a capital breeder. Ecology 94: 1815-1827.
34. Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mammal Sci 26: 509-572.
35. Martinez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84: 91-111.
36. Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: J. B West, G. J Bowen, T. E Dawson and K. P. Tu, editors. Isoscapes. Springer Netherlands. 299-318.
37. Hobson KA, Norris RD (2008) Animal migration: a context for using new techniques and approaches. In: A. H Keith and I. W Leonard, editors. Terrestrial Ecology. Elsevier. 1-19. (Pubitemid 351459593)
38. Adams LG, Dale BW, Mech LD (1995) Wolf predation on caribou calves in Denali National Park, Alaska. In: L. N. Carbyn, S. H. Fritts and D. R. Seip, editors. Ecology and conservation of wolves in a changing world: proceedings of the second North American symposium on wolves. Edmonton, Alberta: University of Alberta. pp. 245-260.
39. Adams LG, Singer FJ, Dale BW (1995) Caribou calf mortality in Denali National Park, Alaska. Journal of Wildlife Management 59: 584-594. (Pubitemid 26450461)
40. Adams LG, Meier T, Owens P, Roffler GH (2006) Interrelationships of Denali's large mammal community. Alaska Park Science 5: 36-40.
41. Adams LG, Dale BW (1998) Reproductive performance of female Alaskan caribou. Journal of Wildlife Management 62: 1184-1195. (Pubitemid 28501636)
42. Miller FL (1974) Age determination of caribou by annulations in dental cementum. Journal of Wildlife Management 38: 47-53.
43. Whitten KR (1995) Antler loss and ydder distension in relation to parturition in caribou. Journal of Wildlife Management 59: 273-277.
44. Nolan JV, Leng RA (1972) Dynamic aspects of ammonia and urea metabolism in sheep. Brit J Nutr 27: 177-193.
45. Gannes LZ, O'Brien DM and Martinez CM (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78: 1271-1276.
46. Ben-David M, Shochat E, Adams LG (2001) Utility of stable isotope analysis in studying foraging ecology of herbivores: examples from moose and caribou. Alces 37: 421-434.
47. Milner JM, Stien A, Irvine RJ, Albon SD, Langvatn R, et al. (2003) Body condition in Svalbard reindeer and the use of blood parameters as indicators of condition and fitness. Canadian Journal of Zoology 81: 1566-1578. (Pubitemid 37546175)
48. Hilderbrand GV, Farley SD, Robbins CT, Hanley TA, Titus K, et al. (1996) Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology 74: 2080-2088.
49. Lobley GE (1994) Amino acid and protein metabolism in the whole body and individual tissues of ruminants. In: J. M. Asplund, editor editors. Priniciples of protein nutrition in ruminants. London, UK: CRC Press. pp. 147-178.
50. Waterlow JC (1999) The mysteries of nitrogen balance. Nutr Res Rev 12: 25-54.
51. Zar JH (1999) Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall. 663 p.
52. Murray K, Conner MM (2009) Methods to quantify variable importance: implications for the analysis of noisy ecological data. Ecology 90: 348-355.
53. Huber PJ, Ronchetti E (2009) Robust statistics. Hoboken, NJ: John Wiley & Sons, Inc.
54. Gustine DD, Barboza PS, Lawler JP, Adams LG, Parker KL, et al. (2012) Diversity of nitrogen isotopes and protein status in caribou: implications for monitoring northern ungulates. Journal of Mammalogy 93: 778-790.
55. Gustine DD, Barboza PS, Adams LG, Farnell RG, Parker KL (2011) An isotopic approach to measuring nitrogen balance in caribou. Journal of Wildlife Management 75: 178-188.
56. Milakovic B, Parker KL (2011) Using stable isotopes to define diets of wolves in northern British Columbia, Canada. Journal of Mammalogy 92: 295-304.
57. Roth JD, Hobson KA (2000) Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Canadian Journal of Zoology-Revue Canadienne De Zoologie 78: 848-852. (Pubitemid 30597459)
58. Lecomte N, Ahlstrøm Ø, Ehrich D, Fuglei E, Ims RA, et al. (2011) Intrapopulation variability shaping isotope discrimination and turnover: experimental evidence in Arctic foxes. Plos One 6: e21357.
59. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94: 189-197.
60. Quillfeldt P, Bugoni L, McGill RR, Masello J, Furness R (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155: 593-598.
61. Sweeting CJ, Barry J, Barnes C, Polunin NVC, Jennings S (2007) Effects of body size and environment on diet-tissue δ15N fractionation in fishes. Journal of Experimental Marine Biology and Ecology 340: 1-10. (Pubitemid 44767761)
62. Adams LG, Farley SD, Stricker CA, Demma DJ, Roffler GH, et al. (2010) Are inland wolf-ungulate systems influenced by marine subsidies of Pacific salmon? Ecological Applications 20: 251-262.
63. Bartz KK, Naiman RJ (2005) Effects of salmon-borne nutrients on riparian soils and vegetation in southwest Alaska. Ecosystems 8: 529-545. (Pubitemid 41346210)
64. Boertje RD (1984) Seasonal diets of the Denali Caribou Herd, Alaska. Arctic 37: 161-165.
65. Fischer LA, Gates CC (2005) Competition potential between sympatric woodland caribou and wood bison in southwestern Yukon, Canada. Canadian Journal of Zoology 83: 1162-1173. (Pubitemid 41712781)
66. Joly K, Cole MJ, Jandt RR (2007) Diets of overwintering caribou, Rangifer tarandus, track decadal changes in Arctic tundra vegetation. The Canadian Field-Naturalist 121: 379-383.
67. Russell DE, Martell AM, Nixon WA (1993) The range ecology of the Porcupine caribou herd in Canada. Rangifer 8: 1-168.
68. Gustine DD, Parker KL, Lay RJ, Gillingham MP, Heard DC (2006) Interpreting resource selection at different scales for woodland caribou in winter. Journal of Wildlife Management 70: 1601-1614. (Pubitemid 46214496)
69. Wang G, Hobbs NT, Boone RB, Illius AW, Gordon IJ, et al. (2006) Spatial and temporal variability modify dependence in populations of large herbivores. Ecology 87: 95-102. (Pubitemid 43363718)
70. Bårdsen BJ, Fauchald P, Tveraa T, Langeland K, Yoccoz NG, et al. (2008) Experimental evidence of a risk-sensitive reproductive allocation in a long-lived mammal. Ecology 89: 829-837. (Pubitemid 351550015)
71. Festa-Bianchet M, Gaillard JM, Jorgenson JT (1998) Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. The American Naturalist 152: 367-379. (Pubitemid 28398074)
72. Robbins CT, Robbins BL (1979) Fetal and neonatal growth patterns and maternal reproductive effort in ungulates and subungulates. The American Naturalist 114: 101-116.
73. Hamel S, Gaillard JM, Festa-Bianchet M, Cote SD (2009) Individual quality, early-life conditions, and reproductive success in contrasted populations of large herbivores. Ecology 90: 1981-1995.
74. McClelland JW, Montoya JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83: 2173-2180. (Pubitemid 36524756)
75. Popp BN, Graham BS, Olson RJ, Hannides CCS, Lott M, et al. (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: T. Dawson and R. Seigwolf, editors. Isotopes as Tracers in Ecological Change. New York, New York: Elsevier. pp. 173-190. (Pubitemid 351734482)
76. O'Brien DM, Boggs CL, Fogel ML (2005) The amino acids used in reproduction by butterflies: A comparative study of dietary sources using compound-specific stable isotope analysis. Physiological and Biochemical Zoology 78: 819-827. (Pubitemid 41292286)
77. Podlesak DW, McWilliams SR (2006) Metabolic routing of dietary nutrients in birds: Effects of diet quality and macronutrient composition revealed using stable isotopes. Physiological and Biochemical Zoology 79: 534-549. (Pubitemid 43846269)
78. O'Brien DM, Fogel ML, Boggs CL (2002) Renewable and nonrenewable resources: Amino acid turnover and allocation to reproduction in lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 99: 4413-4418. (Pubitemid 34285999)
79. 15N in mink. Journal of Mammology 93: 399-412.