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Aspen (Populus tremuloides Michx.) Intake and Preference by Mammalian Herbivores: The Role of Plant Secondary Compounds and Nutritional Context

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Abstract

Aspen (Populus tremuloides Michx.) has evolved a chemical defense system comprised of phenolic glycosides (PG), which effectively deter insect herbivory. However, much less is known about the role of PG and the nutritional quality of the associated plant community on aspen browse susceptibility to mammalian herbivores. In three successive periods during the growing season, we conducted experiments with sheep by offering leaves from two aspen stands with different concentrations of PG (LOW, HIGH) or aspen leaves vs. leaves from a forb (Utah pea, Lathyrus pauciflorus) or a grass (smooth brome, Bromus inermis Leyss.) growing in an aspen understory. Intake of aspen (19 to 35 % PG) was low in all periods (1 to 6 g/Kg0.75 in 2 hr) supporting the notion that aspen’s defense system may contribute to its ecological success. However, lambs ate larger amounts of LOW than of HIGH suggesting that sheep could discriminate between aspen stands with different concentrations of PG, even when both stands were relatively well defended. Concentration of nutrients and chemical defenses in aspen leaves remained fairly stable across the growing season, and preference for aspen increased over the growing season. In contrast, preference for the forb and the grass decreased across the growing season in concert with a decline in the nutritional quality of these plants. The data suggest that nutritional context of aspen and associated forage species drove preference more than contrasts in defense chemistry of aspen. There may be periods of “susceptibility” of aspen use by mammalian herbivores, despite high concentrations of chemical defenses, which can potentially be targeted by management to reduce aspen herbivory.

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References

  • AOAC (2000) Official methods of analysis, 17th edn. Association of official analytical chemists, Gaithersburg

    Google Scholar 

  • Bailey AW, Irving BD, Fitzgerald RD (1990) Regeneration of woody species following burning and grazing in aspen parkland. J Range Manag 43:212–215

    Article  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 Inv 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 

  • Barbehenn RV, Constabel PC (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565

    Article  CAS  PubMed  Google Scholar 

  • Beck JL, Peek JM (2005) Diet composition, forage selection, and potential for forage competition among elk, deer, and livestock on aspen-sagebrush summer range. Range Ecol Manag 58:135–147

    Article  Google Scholar 

  • Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187

    Article  CAS  PubMed  Google Scholar 

  • Behmer ST, Simpson SJ, Raubenheimer D (2002) Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–2501

    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 

  • Cheeke PR, Shull LR (1985) Natural toxicants in feeds and poisonous plants. AVI Publ. Co., Westport

    Google Scholar 

  • Diner B, Berteaux B, Fyles J, Lindroth RL (2009) Behavioral archives link the chemistry and clonal structure of trembling aspen to the food choice of North American porcupine. Oecologia 160:687–695

    Article  PubMed  Google Scholar 

  • Distel EA, Laca EA, Griggs TC, Demment MW (1995) Patch selection by cattle: maximization of intake rate in horizontally heterogeneous pastures. Appl Anim Behav Sci 45:11–21

    Article  Google Scholar 

  • Dockrill CWM, Blenis PIV, Bailey AW, King JR (2004) Effect of summer cattle grazing on aspen stem injury, mortality and growth. Forest Chron 80:257–261

    Article  Google Scholar 

  • Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88:729–739

    Article  PubMed  Google Scholar 

  • Fitzgerald RD, Hudson RJ, Bailey AW (1984) Control of aspen regrowth by grazing with cattle. J Range Manag 37:156–158

    Article  Google Scholar 

  • Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hobbs NT (1996) Modification of ecosystems by ungulates. J Wildl Manag 60:695–713

    Article  Google Scholar 

  • Hobbs NT (2006) Large herbivores as sources of disturbance in ecosystems. In: Danell K, Pastor J, Bergström R, Duncan P (eds) Large herbivore ecology and ecosystem dynamics. Cambridge University Press, Cambridge, pp 261–288

    Chapter  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 

  • Jones B (2010) Restoring aspen under grazed landscapes. PhD Diss. University of California

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

    Article  Google Scholar 

  • Kays JS, Canham CD (1991) Effects of time and frequency of cutting on hardwood root reserves and sprout growth. For Sci 37:524–539

    Google Scholar 

  • Laca EA, Ungar ED, Demment MW (1994) Mechanisms of handling time and intake rate of a large mammalian grazer. Appl Anim Behav Sci 39:3–19

    Article  Google Scholar 

  • Le Gall M, Behmer ST (2011) Nutrient-allelochemical interactions: metabolic effects on a generalist insect herbivore. Ecological Society of America 96th Annual Meetings, Austin, Texas.

  • Lindroth RL (2001) Adaptations of quaking aspen for defense against damage by herbivores and related environmental agents. In: Shepperd WD, Binkley DB, Bartos DL, Stohlgren TJ, Eskew LG (eds), Sustaining aspen in western landscapes: symposium proceedings. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. Fort Collins, pp 273–284

  • Lindroth R, Clair SSB (2013) Adaptation of quaking aspen (Populus tremuloides) for defense against herbivores. For Ecol Manag 299:14–21

    Article  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, 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 

  • Min BR, Barry TN, Attwood GT, McNabb WC (2003) The effects of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim Feed Sci Technol 106:3–19

    Article  CAS  Google Scholar 

  • Nersesian CL, Banks PB, Simpson SJ, McArthur C (2012) Mixing nutrients mitigates the intake constraints of a plant toxin in a generalist herbivore. Behav Ecol 23:879–888

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Porter LJ, Hrstich LN, Chan BC (1986) The conversion of urocyanidins 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 vertebrates: 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 

  • Provenza FD, Burritt EA, Clausen TP, Bryant JP, Reichardt PB, Distel RA (1990) Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. Am Nat 136:810–828

    Article  Google Scholar 

  • Rackham O (2008) Ancient woodlands: modern threats. New Phytol 180:571–586

    Article  PubMed  Google Scholar 

  • Robbins CT, Mole S, Hagerman AE, Hanley TA (1987) Role of tannins in defending plants against ruminants: reduction in dry matter digestion. Ecology 68:1606–1615

    Article  CAS  Google Scholar 

  • Schoenecker KA, Singer FJ, Zeigenfuss LC, Binkley D, Menezes RSC (2004) Effects of elk herbivory on vegetation and nitrogen processes. J Wildl Manag 68:837–849

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Silanikove N, Nitsan Z, Perevolotsky A (1994) Effect of a daily supplementation of polyethylene glycol on intake and digestion of tannin-containing leaves (Ceratonia siliqua) by sheep. J Agric Food Chem 42:2844–2847

    Article  CAS  Google Scholar 

  • Simpson SJ, Raubenheimer D (2001) The geometric analysis of nutrient-allelochemical interactions: a case study using locusts. Ecology 81:422–439

    Google Scholar 

  • Smith AD, Lucas PA, Baker CO, Scotter GW (1972) The effects of deer and domestic livestock on aspen regeneration in Utah. Aspen Bibliography. Paper 5381 http://digitalcommons.usu.edu/aspen_bib/5381

  • Smith EA, Collette SB, Boynton TA, Lillrose T, Stevens MR, Bekker MF, Eggett D, St Clair SB (2011) Developmental contributions to phenotypic variation in functional leaf traits within quaking aspen clones. Tree Physiol 31:68–77

    Article  PubMed  Google Scholar 

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

    CAS  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 

  • Verheyden-Tixier H, Duncan P (2000) Selection for small amounts of hydrolysable tannins by a concentrate-selecting mammalian herbivore. J Chem Ecol 26:351–358

    Article  CAS  Google Scholar 

  • Villalba JJ, Provenza FD (1997a) Preference for wheat straw by lambs conditioned with intraruminal infusions of starch. Br J Nutr 77:287–297

    Article  CAS  PubMed  Google Scholar 

  • Villalba JJ, Provenza FD (1997b) Preference for flavored foods by lambs conditioned with intraruminal administrations of nitrogen. Br J Nutr 78:545–561

    Article  CAS  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 77:378–387

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Villalba JJ, Provenza FD, GouDong H (2004) Experience influences diet mixing by herbivores: implications for plant biochemical diversity. Oikos 107:100–109

    Article  CAS  Google Scholar 

  • Villalba JJ, Provenza FD, Shaw R (2006) Initial conditions and temporal delays influence preference for foods high in tannins and for foraging locations with and without foods high in tannins by sheep. Appl Anim Behav Sci 97:190–205

    Article  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 

  • White CA, Olmsted CE, Kay CE (1998) Aspen, elk, and fire in the Rocky Mountain national parks of North America. Wildl Soc Bull 26:449–462

    Google Scholar 

  • White CA, Feller MC, Bayley S (2003) Predation risk and the functional response of elk–aspen herbivory. Forest 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 30:17–21

    Article  Google Scholar 

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Acknowledgments

Research was supported by grants from the Utah Agricultural Experiment Station, Utah Cooperative Extension and the Utah Division of Wildlife Resources. This paper is published with the approval of the Director, Utah Agricultural Experiment Station, and Utah State University, as journal paper number 8658. We thank the US Forest Service for allowing us collect plant material at the Uintah/Wasatch/Cache National Forest. We also thank A. E. Hagerman and two anonymous referees for helpful comments and suggestions that improved this manuscript. We acknowledge T. Lisonbee, R. Cabassu, V. Egea, Shay Hunt, Tyson Grisenti, and Gavin Johnson for technical support.

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Authors and Affiliations

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

    Juan J. Villalba & Elizabeth A. Burritt

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

    Samuel B. St. Clair

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  1. Juan J. Villalba
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  2. Elizabeth A. Burritt
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Correspondence to Juan J. Villalba.

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Villalba, J.J., Burritt, E.A. & Clair, S.B.S. Aspen (Populus tremuloides Michx.) Intake and Preference by Mammalian Herbivores: The Role of Plant Secondary Compounds and Nutritional Context. J Chem Ecol 40, 1135–1145 (2014). https://doi.org/10.1007/s10886-014-0507-0

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