Is summer food intake a limiting factor for boreal browsers? Diet, temperature, and reproduction as drivers of consumption in female moose


Autoři: Rachel D. Shively aff001;  John A. Crouse aff002;  Dan P. Thompson aff002;  Perry S. Barboza aff001
Působiště autorů: Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas, United States of America aff001;  Alaska Department of Fish and Game, Division of Wildlife Conservation, Kenai Moose Research Center, Soldotna, Alaska, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223617

Souhrn

Food intake may limit the ability of browsing mammals to gain body mass during the growing season when the leaves and stems of woody plants are most abundant. Moose are highly productive browsers with high demands for energy and nutrients, particularly during lactation. Using an indigestible marker, we estimated dry matter intake of free ranging adult female moose with and without calves over three growing seasons. During the same period, we analyzed forage quality. Intakes were highest in late spring (280 ± 19 g·kg-0.75·d-1) when forage quality peaked; however, intakes declined by 39% throughout the summer as temperatures increased and as acid detergent fiber content of browse increased. Digestibility of dry matter declined over summer from 71% to 57% among browse. Intakes were similar for moose with and without calves. Heat loads may impair the ability of moose to consume sufficient energy and nutrients. Warming and habitat change can adversely affect browser populations when poor forage qualities and low dry matter intakes combine to suppress digestible intakes of energy and nutrients.

Klíčová slova:

Diet – Food – Lactation – Nutrients – Phenols – Spring – Moose – Rations


Zdroje

1. Barboza PS, Parker KL, and Hume ID. Integrative Wildlife Nutrition. Springer-Verlag, Heidelberg. 2009.

2. Monteith KL, Klaver RW, Hersey KR, Holland AA, Thomas TP, and Kauffman MJ. Effects of climate and plant phenology on recruitment of moose at the southern extent of their range. Oecologia. 2015; 178:1137–1148. doi: 10.1007/s00442-015-3296-4 25820750

3. Schwartz CC. Physiological and nutritional adaptations of moose to northernenvironments. Alces Suppl. 1992; 1:139–155.

4. Barboza PS, Van Someren LL, Gustine DD, and Bret-Harte MS. The nitrogen window for arctic herbivores: plant phenology and protein gain of migratory caribou (Rangifer tarandus). Ecosphere. 2018; 9(1):e02073. doi: 10.1002/ecs2.2073

5. Gustine DD, Barboza PS, Adams LG, Griffith DB, Cameron RD, and Whitten KR. 2017. Advancing the match-mismatch framework for large herbivores in the Arctic: Evaluating the evidence for a trophic mismatch in caribou. PLOS One 12:1.

6. Johnson HE, Gustine DD, Golden TS, Adams LG, Parrett LS, Lenart EA, et al. 2018. NDVI exhibits mixed success in predicting spatiotemporal variation in caribou summer forage quality and quantity. Ecosphere 9:e02461.

7. Cook JG. 2002. Nutrition and food. Page 259 in Toweill DE and Thomas JW, editors. North American Elk: Ecology and Management. Smithsonian Institution Press, Washington DC.

8. Fulbright TE and Ortega-S JA. 2013. White-tailed Deer Habitat: Ecology and Management on Rangelands. Second edition. Texas A&M University Press, College Station TX.

9. Ahrestani F, Heitkonig IMA, Matsubayashi H, and Prins HHT. 2016. Grazing and browsing by large herbivores in South and Southeast Asia. Page 99 in Ahrestani FS and Sankaran M, editors. The Ecology of Large Herbivores in South and Southeast Asia. Springer Nature, New York, NY.

10. Denryter KA, Cook RC, Cook JG, and Parker KL. 2017. Straight from the caribou’s (Rangifer tarandus) mouth: detailed observations of tame caribou reveal new insights into summer–autumn diets. Canadian Journal of Zoology 95:81.

11. Skarpe C and Hester A. Plant traits, browsing and grazing herbivores, and vegetation dynamics. Page 217 in Gordon IJ, and Prins HHT, editors. The Ecology of Browsing and Grazing. Springer-Verlag, Heidelberg, Germany. 2008.

12. Windels SK and Hewitt DG. Effects of plant secondary compounds on nutritional carrying capacity estimates of a browsing ungulate. Rangeland Ecology and Management. 2011; 64:264.

13. Schwartz CC and Hundertmark KJ. Reproductive characteristics of Alaskan moose. Journal of Wildlife Management. 1993; 57:454–468.

14. Shipley L. Fifty years of food and foraging in moose: lessons in ecology from a model herbivore. Alces. 2010; 46:1–13.

15. Hebblewhite M, Merrill E, and McDermid G. A multi-scale test of the forage maturation hypothesis in a partially migratory ungulate population. Ecological Monographs. 2008; 72:141–166.

16. Murray DL, Cox EW, Ballard WB, Whitlaw HA, Lenarz MS, Custer TW, et al. Pathogens, nutritional deficiency, and climate influences on a declining moose population. Wildlife Monographs. 2006; 166:1–30.

17. Lenarz MS, Nelson ME, Schrage MW, and Edwards AJ. Temperature mediated moose survival in Northeastern Minnesota. Journal of Wildlife Management. 2009; 73:503–510.

18. Sprinkle JE, Holloway JW, Warrington BG, Ellis WC, Stuth JW, Forbes TDA, et al. Digesta kinetics, energy intake, grazing behavior, and body temperature of grazing beef cattle differing in adaptation to heat. Journal of Animal Science. 2000; 78:1608–1624. doi: 10.2527/2000.7861608x 10875645

19. Beale PK, Marsh KJ, Foley WJ, and Moore BD. A hot lunch for herbivores: physiological effects of elevated temperatures on mammalian feeding ecology. Biological Reviews. 2017; 93:674–692. doi: 10.1111/brv.12364 28881466

20. Seaton CT, Paragi TF, Boertje RD, Kielland K, DuBois S, and Fleener CL. Browse biomass removal and nutritional condition of moose Alces alces. Wildlife Biology. 2011; 17:55–66.

21. Paragi TF, Seaton CT, Kellie KA, Boertje RD, Kielland K, Young DD, et al. Browse removal, plant condition, and twinning rates before and after short-term changes in moose density. Alces. 2015; 51:1–21.

22. Parker KL, Barboza PS, and Gillingham MP. Nutrition integrates environmental responses of ungulates. Functional Ecology. 2009; 23:57–69.

23. Bjorneraas K, Herfindal I, Solberg EJ, Saether BE, van Moorter B, and Rolandsen CM. Habitat quality influences population distribution, individual space use and functional responses in habitat selection by a large herbivore. Oecologia. 2012; 168:231–243. doi: 10.1007/s00442-011-2072-3 21766188

24. Wam HK, Felton AM, Stolter C, Nybakken L, and Hjeljord O. Moose selecting for specific nutritional composition of birch places limits on food acceptability. Ecol Evol. 2018; 8:1117–1130. doi: 10.1002/ece3.3715 29375784

25. Renecker LA and Hudson RJ. Seasonal foraging rates of free-ranging moose. Journal of Wildlife Management. 1986; 50:143–147.

26. Dungan JD, Shipley L, and Wright RG. Activity patterns, foraging ecology, and summer range carrying capacity of moose (Alces alces Shirasi) in Rocky Mountain National Park, Colorado. Alces. 2010; 46:71–87.

27. Miquelle DG, Peek JM, and Van Ballenberghe V. Sexual segregation in Alaskan Moose. Wildlife Monographs. 1992; 122:1–57.

28. MacCracken JG, Van Ballenberghe V, and Peek J. M. Habitat relationships of moose on the Copper River delta in coastal south—central Alaska. Wildlife Monographs. 1997; 136:1–52.

29. Renecker LA, and Schwartz CC. Food habits and feeding behavior.in Franzmann AW and Schwartz CC, editors. Ecology and management of the North American moose. Wildlife Management Institute, Washington DC. 1997.

30. Diamond HJ, Karl TR, Palecki MA, Baker CB, Bell JE, Leeper RD, et al. U.S. climate reference network after one decade of operations status and assessment. Bulletin of the American Meteorological Society. 2013; 94:485–498.

31. Miner B. Forest regeneration and use of browse by moose in large-scale wildfires and managed habitat areas, Kenai National Wildlife Refuge, Alaska. Masters of Science, Alaska Pacific University. 2000.

32. Van Soest PJ, Robertson JB, and Lewis BA. Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Science. 1991; 74: 3583–3597.

33. DeGabriel JL, Wallis IR, Moore BD, and Foley WJ. A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia. 2008; 156:107–116. doi: 10.1007/s00442-008-0960-y 18288495

34. VanSomeren LL, Barboza PS, Thompson DP, and Gustine DD. Monitoring digestibility of forages for herbivores: a new application for an old approach. Canadian J. of Zoology. 2015; 93: 187–195.

35. Welch JH, Barboza PS, Farley SD, and Spalinger DE. Nutritional value of habitat for moose on urban military lands. J. Fish and Wildlife Mgmt. 2015; 6:158–175.

36. Sikes RS, and the Animal Care and Use Committee of the American Society of Mammalogists. 2016 guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy. 2016; 97:663–688. doi: 10.1093/jmammal/gyw078 29692469

37. Stephenson TR, Hundertmark KJ, Schwartz CC, and Van Ballenberghe V. Predicting body fat and body mass in moose with ultrasonography. Canadian Journal of Zoology. 1998; 76:717–722.

38. Thompson DP, Crouse JA, McDonough TJ, Badajos OH, Adsem J, and Barboza PS. Vaginal implant transmitters for continuous body temperature measurement in moose. Wildlife Society Bulletin. 2018; 42:321–327.

39. Oftedal OT. Pregnancy and lactation in Bioenergetics of Wild Herbivores, Hudson RJ, White RG, Eds. CRC Press, Boca Raton, FL, pp. 216–238. 1985.

40. Dove H, and Mayes RW. Protocol for the analysis of n-alkanes and other plant-wax compounds and for their use as markers for quantifying the nutrient supply of large mammalian herbivores. Nature Protocols. 2006; 1:1680–1697. doi: 10.1038/nprot.2006.225 17487151

41. Fuller G, Margulis SW, and Santymire R. The effectiveness of indigestible markers for identifying individual animal feces and their prevalence of use in North American zoos. Zoo Biology. 2011; 30:379–398. doi: 10.1002/zoo.20339 20853410

42. Brisson GJ, Pigden WJ, and Sylvestre PE. Effect of frequency of administration of chromic oxide on its fecal excretion pattern by grazing cattle. Canadian Journal of Animal Science. 1957; 37:90–94.

43. Ruggiero LF and Whelan JB. Chromic oxide as an indicator of total fecal output in white-tailed deer. Journal of Range Management. 1977; 30:61–63.

44. Singleton VL, Orthoffer R, and Lamuela-Raventos RM. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology. 1999; 299:152–178.

45. Lauper M, Lechner I, Barboza PB, Collins WB, Hummel J, Codron D, et al. Rumination of different-sized particles in muskoxen (Ovibos moschatus) and moose (Alces alces) on grass and browse diets, and implications for rumination in different ruminant feeding types. Mammalian Biology—Zeitschrift für Säugetierkunde. 2013;78:142–152.

46. Leslie DM Jr., Vavra M, Starkey EE, and Slater RC. Correcting for differential digestibility in microhistological analysis involving common coastal forages of the pacific northwest. Journal of Range Management. 1983; 36:730–732.

47. Huber PJ. The behavior of maximum likelihood estimates under nonstandard conditions. In Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability. Berkeley, CA: University of California Press, vol. 1, 221–233. 1967

48. White H. A heteroskedasticity-consistent covariance matrix estimator and a direct test for heteroskedasticity. Econometrica. 1980; 48: 817–830.

49. Rabe-Hesketh S and Skrondal A. Generalized linear mixed models. International Encyclopedia of Education. 2010; 171–177. doi: 10.1016/B978-0-08-044894-7.01332–4

50. Billor N, Hadi AS, and Velleman PF. BACON: Blocked adaptive computationally efficient outlier nominators. Computational Statistics & Data Analysis. 2000; 34: 279–298.

51. Belsley DA, Kuh E and Welsch RE, “Regression Diagnostics: Identifying Influential Data and Sources of Collinearity,” John Wiley & Sons, Ltd., New York, 1980.

52. Peek JM. A review of moose habitat studies in North America. Le Naturalist Canadien. 1974; 101:195–215.

53. Dungan JD and Wright RG. Summer diet composition of moose in Rocky Mountain National Park, Colorado. Alces. 2005; 41:139–146.

54. LeResche RE and Davis JL. Importance of nonbrowse foods to moose on the Kenai Peninsula, Alaska. The Journal of Wildlife Management. 1973; 37:279–287.

55. Thompson DP and Barboza PS. Seasonal energy and protein requirements for Siberian reindeer (Rangifer tarandus). Journal of Mammalogy. 2017; 98:1558–1567.

56. Bryant JP, Joly K, Chapin FS, DeAngelis DL, and Kielland K. Can antibrowsing defense regulate the spread of woody vegetation in arctic tundra? Ecography. 2014; 37:204–211.

57. Nissinen K, Virjamo V, Randriamanana T, Sobuj N, Sivadasan U, Mehtatalo L, et al. Responses of growth and leaf phenolics in European aspen (Populus tremula) to climate change during juvenile phase change. Canadian Journal of Forest Restoration. 2017; 47:1350–1363.

58. Austin PJ, Suchar LA, Robbins CT, and Hagerman AE. Tannin-binding proteins in saliva of sheep and deer and their absence in saliva of sheep and cattle. Journal of Chemical Ecology. 1989; 15:1335–1347. doi: 10.1007/BF01014834 24272016

59. Hagerman AE and Robbins CT. Specificity of tannin-binding salivary proteins relative to diet selection by mammals. Canadian Journal of Zoology. 1993; 71:628–633.

60. Juntheikki MR. Comparison of tannin-binding proteins in saliva of Scandinavian and North American moose (Alces alces). Biochemical Systematics and Ecology. 1996; 24:595–601.

61. Klein DR. Variation in quality of caribou and reindeer forage plants associated with season, plant part, and phenology. Rangifer Speicial. 1990; I:123–130.

62. Schwartz CC, Regelin WL, and Franzmann AW. Seasonal dynamics of food intake in moose. Alces. 1984; 20:223–244.

63. Shipley LA and Spalinger DE. Mechanics of browsing in dense food patches: effect of plant and animal morphology on intake rate. Canadian Journal of Zoology. 1992; 70:1743–1752.

64. Renecker LA and Hudson RJ. Seasonal activity budgets of moose in aspen-dominated boreal forests. Journal of Wildlife Management. 1989; 53:296–302.

65. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Krizsan SJ, Hedwall PO, et al. The nutritional balancing act of a large herbivore: an experiment with captive moose (Alces alces L). PLoS ONE. 2016; 11(3): e0150870. doi: 10.1371/journal.pone.0150870 26986618

66. Schwartz CC, Hunnert ME, and Franzmann AW. Energy requirements of adult moose for winter maintenance. The Journal of Wildlife Management. 1988; 52:26–33.

67. Timmerman HR and McNicol JG. Moose habitat needs. Canadian Institute of Forestry, The Forestry Chronicle June 1988:238–245.

68. Schwartz CC, Regelin WL, and Franzmann AW. Digestion in moose. The Journal of Wildlife Management. 1987; 51:352–357.

69. McArt SH, Spalinger DE, Collins WB, Schoen ER, Stevenson T, and Bucho M. Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central Alaska. Ecology. 2009; 90:1400–1411. doi: 10.1890/08-1435.1 19537559

70. Hamel S and Cote S. Foraging decisions in a capital breeder: trade-offs between mass gain and lactation. Oecologia. 2009; 161:421–432. doi: 10.1007/s00442-009-1377-y 19488787

71. Lechner I, Barboza PS, Collins W, Fritz J, Gunther D, Hattendorf B, et al. Differential passage of fluids and different-sized particles in fistulated oxen (Bos primigenius f. taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces): Rumen particle size discrimination is independent from contents stratification. Comparative Biochemistry and Physiology A. 2010;155:211–222.

72. Broders HG, Coombs AB, and McCarron JR. Ectothermic responses of moose (Alces alces) to thermoregulatory stress on mainland Nova Scotia. Alces. 2012; 48:53–61.

73. Joly K, Duffy PA, and Rupp TS. Simulating the effects of climate change on fire regimes in Arctic biomes: implications for caribou and moose habitat. Ecosphere. 2012; 3:36.

74. Dou H, Jiang G, Stott P, and Piao R. Climate change impacts population dynamics and distribution shift of moose (Alces alces) in Heilongjiang Province of China. Ecol Res. 2013; 28:625–632.

75. McCann NP, Moen RA, and Harris TR. Warm-season heat stress in moose (Alces alces). Canadian Journal of Zoology. 2013; 91:893–898.

76. Melin M, Matala J, Mehtatalo L, Tiilikainen R, Tikkanen O, Maltamo M, et al. Moose (Alces alces) reacts to high summer temperatures by utilizing thermal shelters in boreal forests–an analysis based on airborne laser scanning of the canopy structure at moose locations. Global Change Biology. 2014; 20:1115–1125. doi: 10.1111/gcb.12405 24115403

77. Tape KD, Gustine DD, Ruess RW, Adams LG, and Clark JA. Range expansion of moose in Arctic Alaska linked to warming and increased shrub habitat. PLoS ONE. 2016; 11:1–12.

78. Hoy SR, Peterson RO, and Vucetich JA. Climate warming is associated with smaller body size and shorter lifespans in moose near their southern range limit. Global Change Biology. 2017; 00:1–10. https://doi.org/10.1111/gcb.14015.

79. Street GM, Fieberg J, Rodgers AR, Carstensen M, Moen R, Moore SA, et al. Habitat functional response mitigates reduced foraging opportunity: implications for animal fitness and space use. Landscape Ecology. 2016; 31:1939–1953.

80. Ditmer MA, Moen RA, Windels SK, Forester JD, Ness TE, and Harris TR. Moose at their bioclimatic edge alter their behavior based on weather, landscape, and predators. Current Zoology. 2017; 1–14.

81. Allman BP, Kielland K, and Wagner D. Leaf herbivory by insects during summer reduces overwinter browsing by moose. BMC Ecology. 2018; 18:38. doi: 10.1186/s12898-018-0192-x 30261869

82. Zarnke RL, Samuel WM, Franzmann AW, and Barrett R. Factors influencing the potential establishment of the winter tick (Dermacentor albipictus) in Alaska. Journal of Wildlife Diseases. 1990; 26:412–415. doi: 10.7589/0090-3558-26.3.412 2388366

83. DelGiudice GD, Peterson RO, and Samuel WM. Trends of winter nutritional restriction, ticks, and numbers of moose on Isle Royale. The Journal of Wildlife Management. 1997; 61:895–903.

84. Mooring MS and Samuel WM. Premature loss of winter hair in free-ranging moose (Alces alces) infested with winter ticks (Dermacentor albipictus) is correlated with grooming rate. Canadian Journal of Zoology. 1999; 77:148–156.

85. Samuel B. White as a ghost: winter ticks and moose. Nature Alberta. 2004 100 pp.

86. Durden LA, Beckman KB, and Gerlach RF. New records of ticks (Acari: Ixodidae) from dogs, cats, humans, and some wild vertebrates in Alaska: Invasion potential. Journal of Medical Entomology. 2016; 53:1391–1395. doi: 10.1093/jme/tjw128 27524823

87. Flook DR. 1959. Moose using water as a refuge from flies. Journal of Mammalogy 40:455.8. Fulbright TE and Ortega-S JA. White-tailed Deer Habitat: Ecology and Management on Rangelands. Second edition. Texas A&M University Press, College Station TX. 2013.

88. Renecker LA and Hudson RJ. Behavioral and thermoregulatory responses of moose to high ambient temperatures and insect harassment in aspen-dominated forests. Alces. 1990; 26:66–72.


Článek vyšel v časopise

PLOS One


2019 Číslo 10

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Léčba bolesti v ordinaci praktického lékaře
nový kurz
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Léčba akutní pooperační bolesti
Autoři: doc. MUDr. Jiří Málek, CSc.

Nové antipsychotikum kariprazin v léčbě schizofrenie
Autoři: prof. MUDr. Cyril Höschl, DrSc., FRCPsych.

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se