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Plant Community Chemical Composition Influences Trembling Aspen (Populus tremuloides) Intake by Sheep

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Abstract

Nutrients and plant secondary compounds in aspen (Populus tremuloides) may interact with nutrients in the surrounding vegetation to influence aspen use by herbivores. Thus, this study aimed to determine aspen intake and preference by sheep in response to supplementary nutrients or plant secondary compounds (PSC) present in aspen trees. Thirty-two lambs were randomly assigned to one of four molasses-based supplementary feeds to a basal diet of tall fescue hay (N = 8) during three experiments. The supplements were as follows: (1) high-protein (60% canola meal), (2) a PSC (6% quebracho tannins), (3) 25% aspen bark, and (4) control (100% molasses). Supplements were fed from 0700 to 0900, then lambs were fed fresh aspen leaves collected from stands containing high (Experiment 1, 2) or low (Experiment 3) concentrations of phenolic glycosides (PG). In Experiment 2, lambs were simultaneously offered aspen, a forb (Lathyrus pauciflorus), and a grass (Bromus inermis) collected from the aspen understory. Animals supplemented with high protein or tannins showed greater intake of aspen leaves than animals supplemented with bark or the control diet (P < 0.05), likely because some condensed tannins have a positive effect on protein nutrition and protein aids in PSC detoxification. Overall, animals supplemented with bark showed the lowest aspen intake, suggesting PSC in bark and aspen leaves had additive inhibitory effects on intake. In summary, these results suggest that not only the concentration but also the types and proportions of nutrients and chemical defenses available in the plant community influence aspen use by herbivores.

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References

  • AOAC (2000) Official methods of analysis, 17th edn. Association of official analytical chemists. Perkin Elmer 5300 DV ICP. Perkin Elmer, 710 Bridgeport avenue, Shelton, CT 06484

  • Atsatt PR, O’Dowd DJ (1976) Plant defense guilds. Science 193(4247):24–29

    Article  CAS  PubMed  Google Scholar 

  • Bailey JK, Schweitzer JA, Rehill BJ, Irschick DJ, Whitham TG, Lindroth RL (2007) Rapid shifts in the chemical composition of aspen forests: an introduced herbivore as an agent of natural selection. Biol Invasions 9:715–722

    Article  Google Scholar 

  • Baraza E, Villalba JJ, Provenza FD (2005) Nutritional context influences preferences of lambs for foods with plant secondary metabolites. Appl Anim Behav Sci 92:293–305

    Article  Google Scholar 

  • Baraza E, Zamora R, Hódar JA (2006) Conditional outcomes in plant–herbivore interactions: neighbours matter. Oikos 113:148–156

    Article  Google Scholar 

  • Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509

    Article  CAS  PubMed  Google Scholar 

  • Bryant JP, Kuropat PJ (1980) Selection of winter forage by subarctic browsing vertebrates: the role of plant chemistry. Annu Rev Ecol Syst 11(1):261–285

    Article  CAS  Google Scholar 

  • Burritt EA, Provenza FD (2000) Role of toxins in intake of varied diets by sheep. J Chem Ecol 26(8):1991–2005

    Article  CAS  Google Scholar 

  • Cardozo PW, Calsamiglia S, Ferret A, Kamel C (2004) Effects of natural plant extracts on ruminal protein degradation and fermentation profiles in continuous culture. J Anim Sci 82(11):3230–3236

    Article  CAS  PubMed  Google Scholar 

  • Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189

    Article  Google Scholar 

  • Donaldson JR, Stevens MT, Barnhill HR, Lindroth RL (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J Chem Ecol 32:1415–1429

    Article  CAS  PubMed  Google Scholar 

  • Erbilgin N, Galvez DA, Zhang B, Najar A (2014) Resource availability and repeated defoliation mediate compensatory growth in trembling aspen (Populus tremuloides) seedlings. Peer J 2:e491. doi:10.7717/peerj.491

    Article  PubMed  PubMed Central  Google Scholar 

  • Foley WJ, Iason GR, McArthur C (1999) Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: Jung HJG and Fahey GC Jr. (eds) Nutritional ecology of herbivores. American Socitey of Animal Science. Savoy, Il, pp 130–209

  • Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–288

    Article  CAS  Google Scholar 

  • Frutos P, Hervás G, Giráldez FJ, Mantecón AR (2004) Review. Tannins and ruminant nutrition. Span J Agric Res 2(2):191–202

    Article  Google Scholar 

  • Hagerman AE, Butler L (1980) Condensed tannin purification and characterization of tannin-associated proteins. J Agric Food Chem 28:947–952

    Article  CAS  PubMed  Google Scholar 

  • Hagerman AE, Robbins CT, Weerasuriya Y, Wilson TC, McArthur C (1992) Tannin chemistry in relation to digestion. J Range Manag 45:57–62

    Article  Google Scholar 

  • Hamilton T, Burritt EA, Villalba JJ (2015) Assessing the impact of supplements, food aversions, andsilica on medusahead (Taeniatherum caput-medusae (L.) Nevski) use by sheep. Small Rumin Res 124:45–54

    Article  Google Scholar 

  • Harper AE (1974) Amino acid excess. In: White PL and Fletcher DC (eds) Nutrients in processed foods—proteins. Publishing Sciences Group, Acton, MA

  • Hemming JDC, Lindroth RL (2000) Effects of phenolic glycosides and protein on gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) performance and detoxication activities. Environ Entomol 29:1108–1115

    Article  CAS  Google Scholar 

  • Heroy KY (2017) The influence of aspen chemistry and the nutritional context on aspen herbivory. Dissertation, Utah State University

  • Hjältén J, Danell K, Lundberg P (1993) Herbivore avoidance by association: vole and hare utilization of woody plants. Oikos 1:125–131

    Article  Google Scholar 

  • Holeski LM, McKenzie SC, Kruger EL, Couture JJ, Rubert-Nason K, Lindroth RL (2016) Phytochemical traits underlie genotypic variation in susceptibility of quaking aspen (Populus tremuloides) to browsing by a keystone forest ungulate. J Ecol 104:850–863

    Article  Google Scholar 

  • Illius AW, Jessop NS (1995) Modeling metabolic costs of allelochemical ingestion by foraging herbivores. J Chem Ecol 21:693–719

    Article  CAS  PubMed  Google Scholar 

  • Illius AW, Jessop NS (1996) Metabolic constraints on voluntary intake in ruminants. J Anim Sci 74:3052–3062

    Article  CAS  PubMed  Google Scholar 

  • Jones BE, Lile DF, Tate KW (2011) Cattle selection for aspen and meadow vegetation: implications for restoration. Rangel Ecol Manag 64:625–632

    Article  Google Scholar 

  • Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD (2014) Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett 17(10):1238–1246

    Article  PubMed  Google Scholar 

  • Leimar O, Tuomi J (1998) Synergistic selection and graded traits. Evol Ecol 12:59–71

    Article  Google Scholar 

  • Lindroth RL, Bloomer MS (1991) Biochemical ecology of the forest tent caterpillar: responses to dietary protein and phenolic glycosides. Oecologia 86(3):408–413

    Article  PubMed  Google Scholar 

  • Lindroth RL, Hwang SY (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions. Plenum Press, New York, pp 25–56

    Chapter  Google Scholar 

  • Lindroth RL, Pajutee MS (1987) Chemical analysis of phenolic glycosides: art, facts, and artifacts. Oecologia 74:144–148

    Article  CAS  PubMed  Google Scholar 

  • Lindroth RL, St. Clair SB (2013) Adaptations of quaking aspen (Populus Tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21

    Article  Google Scholar 

  • Lindroth RL, Kinney KK, Platz CL (1993) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry, and insect performance. Ecology 74:763–777

    Article  CAS  Google Scholar 

  • MacAdam JW, Villalba JJ (2015) Beneficial effects of temperate forage legumes that contain condensed tannins. Agriculture 20:475–491

    Article  Google Scholar 

  • Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87(8):2103–2112

    Article  PubMed  Google Scholar 

  • NRC (1985) Nutrient requirements of sheep, 6th edn. National Academy Press, Washington

    Google Scholar 

  • Odenyo AA, Osuji PO (1998) Tannin-tolerant ruminal bacteria from east African ruminants. Can J Microbiol 44:904–909

    Article  Google Scholar 

  • Palo RT, Robbins CT (1991) Plant defenses against mammalian herbivory. CRC Press, Boca Raton

    Google Scholar 

  • Pass G, Foley WJ (2000) Plant secondary metabolites as mammalian feeding deterrents: separating the effects of the taste of salicin from its post-ingestive consequences in the common brushtail possum (Trichosurus vulpecula). J Comp Physiol B 170(3):185–192

    Article  CAS  PubMed  Google Scholar 

  • Porter LJ, Hrstich LN, Chan BC (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

    Article  CAS  Google Scholar 

  • Provenza FD (1995) Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J Range Manag 48:2–17

    Article  Google Scholar 

  • Provenza FD, Villalba JJ (2006) Foraging in domestic herbivores: linking the internal and external milieu. In: Bels VL (ed) Feeding in domestic vertebrates: from structure to function. CABI Publ, Oxfordshire, pp 210–240

    Chapter  Google Scholar 

  • Rautio P, Kesti K, Bergvall UA, Tuomi J, Leimar O (2008) Spatial scales of foraging in fallow deer: implications for associational effects in plant defences. Oecologica 34(1):12–20

    Article  Google Scholar 

  • Rautio P, Bergvall UA, Tuomi J, Kesti K, Leimar O (2012) Food selection by herbivores and neighbourhood effects in the evolution of plant defences. Ann Zool Fenn 49(1–2):45–57

    Article  Google Scholar 

  • Reed JD (1995) Nutritional toxicology of tannins and related polyphenols in forage legumes. J Anim Sci 73:1516–1528

    Article  CAS  PubMed  Google Scholar 

  • Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107

    Article  CAS  Google Scholar 

  • Robbins CT, Hagerman AE, Austin PJ, McArthur C, Hanley TA (1991) Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J Mammal 72:480–486

    Article  Google Scholar 

  • Seager ST, Eisenberg C, St. Clair SB (2013) Patterns and consequences of ungulate herbivory on aspen in western North America. For Ecol Manag 299:81–90

    Article  Google Scholar 

  • Senft RL, Coughenour MB, Bailey DW, Rittenhouse LR, Sala OE, Swift DM (1987) Large herbivore foraging and ecological hierarchies. Bioscience 37:789–799

    Article  Google Scholar 

  • Swift RW (1957) The caloric value of TDN. J Anim Sci 16:753–756

    Article  CAS  Google Scholar 

  • Van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Cornell University Press, Ithaca

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Villalba JJ, Provenza FD (1999) Nutrient-specific preferences by lambs conditioned with intraruminal infusions of starch, casein, and water. J Anim Sci 77(2):378–387

    Article  CAS  PubMed  Google Scholar 

  • Villalba JJ, Provenza FD (2002) Consequences of the interaction between nutrients and plant secondary metabolites on herbivore selectivity: benefits or detriments for plants? Oikos 97(2):282–292

    Article  CAS  Google Scholar 

  • Villalba JJ, Provenza FD (2005) Foraging in chemically diverse environments: energy, protein, and alternative foods influence ingestion of plant secondary metabolites by lambs. J Chem Ecol 31(1):123–138

    Article  CAS  PubMed  Google Scholar 

  • Villalba JJ, Provenza FD, Banner RE (2002) Influence of macronutrients and polyethylene glycol on intake of a quebracho tannin diet by sheep and goats. J Anim Sci 80:3154–3164

    Article  CAS  PubMed  Google Scholar 

  • Villalba JJ, Provenza FD, Hall JO (2008) Learned appetites for calcium, phosphorus, and sodium in sheep. J Anim Sci 86(3):738–747

    Article  CAS  PubMed  Google Scholar 

  • Villalba JJ, Burritt EA, St. Clair SB (2014) Aspen (Populus tremuloides Michx.) intake and Ppference by mammalian herbivores: the role of plant secondary compounds and nutritional context. J Chem Ecol 40(10):1135–1145

    Article  CAS  PubMed  Google Scholar 

  • Villalba JJ, Provenza FD, Catanese F, Distel RA (2015) Understanding and manipulating diet choice in grazing animals. Anim Prod Sci 55:261–271

    Article  CAS  Google Scholar 

  • Waghorn G (2008) Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production—progress and challenges. Anim Feed Sci Technol 147:116–139

    Article  CAS  Google Scholar 

  • Weiss WP, Conrad HR, Pierre NRS (1992) A theoretically-based model for predicting total digestible nutrient values of forages and concentrates. Anim Feed Sci Technol 39:95–110

    Article  CAS  Google Scholar 

  • Westoby M (1978) What are the biological bases of varied diets? Am Nat 112:627–631

    Article  Google Scholar 

  • White CA, Feller MC, Bayley S (2003) Predation risk and the functional response of elk-aspen herbivory. For Ecol Manag 181:77–97

    Article  Google Scholar 

  • Wooley SC, Walker S, Vernon J, Lindroth RL (2008) Aspen decline, aspen chemistry, and elk herbivory: are they linked? Rangelands 30(1):17–21

    Article  Google Scholar 

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Acknowledgements

This research was supported by grants from Utah State University, School of Graduate Studies (SPARC), The Ecology Center, and the Utah Agricultural Experiment Station. This paper is published with the approval of the Director, Utah Agricultural Experiment Station, and Utah State University, as journal paper number 9003.

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Authors and Affiliations

  1. Department of Wildland Resources, Utah State University, Logan, 84322-5230, USA

    Kristen Y. Heroy, Elizabeth A. Burritt & Juan J. Villalba

  2. Department of Plant & Wildlife Sciences, Brigham Young University, Provo, UT, 84602, USA

    Samuel B. St. Clair

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  1. Kristen Y. Heroy
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  2. Samuel B. St. Clair
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  3. Elizabeth A. Burritt
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Correspondence to Kristen Y. Heroy.

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This study was funded by the Utah State Agricultural Research Experiment Station (grant number 1068).

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Heroy, K.Y., St. Clair, S.B., Burritt, E.A. et al. Plant Community Chemical Composition Influences Trembling Aspen (Populus tremuloides) Intake by Sheep. J Chem Ecol 43, 817–830 (2017). https://doi.org/10.1007/s10886-017-0872-6

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  • DOI: https://doi.org/10.1007/s10886-017-0872-6

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