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Differences in Vole Preference, Secondary Chemistry and Nutrient Levels Between Naturally Regenerated and Planted Norway Spruce Seedlings

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Abstract

Field voles (Microtus agrestis) cause severe damage to young Norway spruce (Picea abies) plantations during wintertime in Fennoscandia. We experimentally investigated vole preference for winter-dormant, naturally regenerated seedlings; spring-planted seedlings; or autumn-planted seedlings; and how preference corresponds with seedling chemistry. Voles showed the highest preference for autumn-planted seedlings and the second highest for spring-planted seedlings, while naturally regenerated seedlings were avoided. The stems of the autumn-planted seedlings contained higher concentrations of nitrogen and piperidine alkaloids and lower concentrations of stilbenes than did the other groups. In addition to differences between naturally regenerated and planted seedlings, we investigated seasonal differences in naturally regenerated P. abies needle and bark secondary chemistry. While piperidine alkaloid concentrations did not vary with season, the soluble non-tannin phenolics of needles and the condensed tannins of bark were lower in May than in November or January. At the time of planting, the concentration of bark piperidine alkaloids was higher in autumn-planted than in spring-planted seedlings. We detected two alkaloids not previously found in P. abies, 2-methyl-6-propyl-1,6-piperideine and a tentatively identified pinidine-isomer. Our results demonstrate that vole choice of spruce seedlings is promoted by high nitrogen and low stilbene content, both associated with seedlings planted late in the season. As vole damage is linked to seedling chemistry, damage potentially could be mitigated by advancing planting or by manipulating plant chemistry in nurseries.

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References

  • Baxter R, Hansson L (2001) Bark consumption by small rodents in the northern and southern hemispheres. Mammal Rev 31:47–59

    Article  Google Scholar 

  • Brown HC, Racherla US (1986) Organoboranes. 43. A convenient, highly efficient synthesis of triorganylboranes via a modified organometallic route. J Org Chem 51:427–432

    Article  CAS  Google Scholar 

  • Bubnov YN, Klimkina EV, Ignatenko AV (1998) Preparation of trans- and cis-2-allyl-6-alkyl(aryl)-1,2,3,6-tetrahydropyridines based on the reductive trans-2,6-dialkylation of pyridine. Synthesis of (±)-epidihydropinidine and (±)-dihydropinidine. Russ Chem Bull 47:451–458

    Article  CAS  Google Scholar 

  • Chen W, Liu Y, Chen Z (2005) A highly efficient and practical new allylboronate tartramide for the asymmetric allylboration of achiral aldehydes. Eur J Org Chem 8:1665–1668

    Article  Google Scholar 

  • Clausen TP, Reichardt PB, Bryant JP (1986) Pinosylvin and pinosylvin methyl ether as feeding deterrents in green alder. J Chem Ecol 12:2117–2131

    Article  CAS  Google Scholar 

  • Danell K, Elmqvist T, Ericson L, Salomonson A (1987) Are there general patterns in bark-eating by voles on different shoot types from woody-plants. Oikos 50:396–402

    Article  Google Scholar 

  • Fischbach RJ, Kossmann B, Panten H, Steinbrecher R, Heller W, Seidlitz HK, Sandermann H, Hertkorn N, Schnitzler JP (1999) Seasonal accumulation of ultraviolet-B screening pigments in needles of Norway spruce (Picea abies (L.) Karst.). Plant Cell Environ 22:27–37

    Article  CAS  Google Scholar 

  • Gali-Muhtasib HU, Smith CC, Higgins JJ (1992) The effect of silica grasses on the feeding behavior of prairie vole, Microtus Ochrogaster. Ecology 73:1724–1729

    Article  Google Scholar 

  • Gerson EA, Kelsey RG (1998) Variation of piperidine alkaloids in ponderosa (Pinus ponderosa) and lodgepole pine (P. contorta) foliage from central Oregon. J Chem Ecol 24:815–827

    Article  CAS  Google Scholar 

  • Gerson EA, Kelsey RG (1999a) Piperidine alkaloids in nitrogen fertilized Pinus ponderosa. J Chem Ecol 25:2027–2039

    Article  CAS  Google Scholar 

  • Gerson EA, Kelsey RG (1999b) Foliar storage and extraction methods for quantitative analysis of piperidine alkaloids from Ponderosa pine (Pinus ponderosa). Phytochem Anal 10:322–327

    Article  CAS  Google Scholar 

  • Gerson EA, Kelsey RG (2002) Piperidine alkaloids in sitka spruce with varying levels of resistance to white pine weevil (Coleoptera: Curculionidae). J Econ Entomol 95:608–613

    Article  PubMed  CAS  Google Scholar 

  • Gerson EA, Kelsey RG (2004) Piperidine alkaloids in North American Pinus taxa: implications for chemosystematics. Biochem Syst Ecol 32:62–74

    Article  Google Scholar 

  • Gerson EA, Kelsey RG, St Clair JB (2009) Genetic variation of piperidine alkaloids in Pinus ponderosa: a common garden study. Ann Bot 103:447–457

    Article  PubMed  CAS  Google Scholar 

  • Gill RMA (1992) A Review of damage by mammals in north temperate forest. 2. Small Mammals. Forestry 65:281–308

    Article  Google Scholar 

  • Hagerman AE (2002) The tannin handbook. (updated: 2011). Department of Chemistry & Biochemistry, Miami University, Oxford, OH 45056. http://www.users.muohio.edu/hagermae/

  • Hansson L (1992) Vole densities and consumption of bark in relation to soil type and bark mineral content. Scand J Forest Res 7:229–235

    Article  Google Scholar 

  • Harju A, Tahvanainen J (1994) The effect of silver birch (Betula pendula) powder on physiological performance of field voles (Microtus agrestis). Ann Zool Fennici 31:229–234

    Google Scholar 

  • Hartley SE, Nelson K, Gorman M (1995) The effect of fertilizer and shading on plant chemical composition and palatability to Orkney voles, Microtus arvalis orcadensis. Oikos 72:79–87

    Article  Google Scholar 

  • Heiska S, Tikkanen OP, Rousi M, Julkunen-Tiitto R (2008) Bark salicylates and condensed tannins reduce vole browsing amongst cultivated dark-leaved willows (Salix myrsinofolia). Chemoecology 17:245–253

    Article  Google Scholar 

  • Heroldová M, Bryja J, Jánová E, Suchomel J, Homolka M (2012) Rodent damage to natural and replanted mountain forest regeneration. Sci World J. doi:10.1100/2012/872536

    Google Scholar 

  • Hjältén J, Palo T (1992) Selection of deciduous trees by free ranging voles and hares in relation to plant chemistry. Oikos 63:477–484

    Article  Google Scholar 

  • Hjältén J, Danell K, Ericson L (2004) Hare and vole browsing preferences during winter. Acta Theriol 49:53–62

    Article  Google Scholar 

  • Hodson MJ, Sangster AG (1999) Aluminium/silicon interactions in conifers. J Inorg Biochem 76:89–98

    Article  CAS  Google Scholar 

  • Huitu O, Kiljunen N, Korpimäki E, Koskela E, Mappes T, Pietiäinen H, Pöysä H, Henttonen H (2009) Density-dependent vole damage in silviculture and associated economic losses at a nation wide scale. Forest Ecol Manag 258:1219–1224

    Article  Google Scholar 

  • Julkunen-Tiitto R, Sorsa S (2001) Testing the effects of drying methods on willow flavonoids, tannin and salicylates. J Chem Ecol 27:779–789

    Article  PubMed  CAS  Google Scholar 

  • Julkunen-Tiitto R, Rousi M, Bryant J, Sorsa S, Sikanen H, Keinänen M (1996) Chemical diversity of Betulaceae species: comparison of phenolics and terpenoids in northern birch species. Trees 11:16–22

    Article  Google Scholar 

  • Marquis RJ, Batzli GO (1989) Influence of chemical factors on palatability of forage to voles. J Mamm 79:503–511

    Article  Google Scholar 

  • Massey FP, Ennos AR, Hartley SE (2007) Grasses and the resource availability hypothesis: the importance of silica-based defences. J Ecol 95:414–424

    Article  CAS  Google Scholar 

  • Massey FP, Hartley SE (2006) Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates. P R Soc B 273:2299–2304

    Article  CAS  Google Scholar 

  • Massey FP, Smith MJ, Lambin X, Hartley SE (2008) Are silica defences in grasses driving vole population cycles? Biol Lett 4:419–422

    Article  PubMed  CAS  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Syst 11:119–161

    Article  Google Scholar 

  • Nilsson U, Luoranen J, Kolström T, Örlander G, Puttonen P (2010) Reforestation with planting in northern Europe. Scand J For Res 25:283–294

    Article  Google Scholar 

  • Nordborg F, Nilsson U (2003) Growth, damage and net nitrogen uptake in Picea abies (L.) Karst. seedlings, effects of site preparation and fertilisation. Ann For Sci 60:657–666

    Article  Google Scholar 

  • Nybakken L, Hörkkä R, Julkunen-Tiitto R (2012) Combined enhancements of temperature and UVB influence growth and phenolics in clones of the sexually dimorphic Salix myrsinifolia. Physiol Plant 145:551–564

    Article  PubMed  CAS  Google Scholar 

  • Pan H, Lundgren L (1985) Phenolic extractives from root bark of Picea abies. Phytochemistry 39:1423–1428

    Article  Google Scholar 

  • Pusenius J, Prittinen K, Heimonen J, Koivunoro K, Rousi M, Roininen H (2002) Choice of voles among genotypes of birch seedlings: its relationship with seedling quality and preference of insects. Oecologia 130:426–432

    Article  Google Scholar 

  • Rousi M, Tahvanainen J, Henttonen H, Uotila I (1993) The effect of shading and fertilization on the resistance of winter-dormant European white birch (Betula pendula) to vole and hare feeding. Ecology 74:30–38

    Article  Google Scholar 

  • Roy J, Bergeron JM (1990) Role of phenolics of coniferous trees as deterrents against debarking behavior of meadow voles (Microtus pennsylvanicus). J Chem Ecol 16:801–808

    Article  Google Scholar 

  • Rummukainen A, Julkunen-Tiitto R, Räisänen M, Lehto T (2007) Phenolic compounds in Norway spruce as affected by boron nutrition at the end of growing season. Plant Soil 292:13–23

    Article  CAS  Google Scholar 

  • Schiebe C, Hammerbacher A, Birgersson G, Witzell J, Brodelius PE, Gershenzon J, Hansson BS, Krokene P, Schlyter F (2012) Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia 170:183–198

    Article  PubMed  Google Scholar 

  • Schneider MJ, Montali JA, Hazen D, Stanton CE (1991) Alkaloids of Picea. J Nat Prod 54:905–909

    Article  CAS  Google Scholar 

  • Solhaug KA (1990) Stilbene glucosides in bark and needles from Picea species. Scand J For Res 5:59–67

    Article  Google Scholar 

  • Stermitz FR, Tawara JN, Boeckl M, Pomeroy M, Foderaro TA, Todd FG (1994) Piperidine alkaloid content of Picea (spruce) and Pinus (pine). Phytochemistry 35:951–953

    Article  CAS  Google Scholar 

  • Stermitz FR, Kamm CD, Tawara JN (2000) Piperidine alkaloids of spruce (Picea) and fir (Abies) species. Biochem Syst Ecol 28:177–181

    Article  CAS  Google Scholar 

  • Strack D, Heilemann J, Wray V, Dirks H (1989) Structure and accumulation patterns of soluble and insoluble phenolics from Norway spruce needles. Phytochemistry 28:2071–2078

    Article  CAS  Google Scholar 

  • Sullivan TP, Martin WL (1991) Influence of site factors on incidence of vole and lemming feeding damage to forest plantations. West J Appl For 6:64–67

    Google Scholar 

  • Sullivan TP, Sullivan DS (2010) Forecasting vole population outbreaks in forest plantations: the rise and fall of a major mammalian pest. For Ecol Manag 260:983–993

    Article  Google Scholar 

  • Tawara JN, Blokhin A, Foderaro TA, Stermitz FR, Hope H (1993) Toxic piperidine alkaloids from pine (Pinus) and spruce (Picea) trees. New structures and a biosynthetic hypothesis. J Org Chem 58:4813–4818

    Article  CAS  Google Scholar 

  • Todd FG, Stermitz FR, Blokhin AV (1995) Piperidine alkaloid content of Picea pungens (Colorado blue spruce). Phytochemistry 40:401–406

    Article  CAS  Google Scholar 

  • Viiri H, Annila E, Kitunen V, Niemelä P (2001) Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15:112–122

    Article  CAS  Google Scholar 

  • Wink M, Meissner C, Witte L (1995) Patterns of quinolizidine alkaloids in 56 species of the genus Lupinus. Phytochemistry 38:139–153

    Article  CAS  Google Scholar 

  • Yamazaki N, Kibayashi C (1989) Asymmetric synthesis with α, β-bis[(methoxymethyl)oxy] ketones. Enantioselective total synthesis of natural (+)-indolizidine 195B (bicyclic gephyrotoxin 195B) and (−)-pinidine and their enantiomers from a common chiral synthon. J Am Chem Soc 111:1396–1408

    Article  CAS  Google Scholar 

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Acknowledgments

We acknowledge Riitta Pietarinen, Anu Lavola, and Milla Ratilainen for assistance in the laboratory analyses. The English was checked by Rosemary Mackenzie, M.A.. This work was financially supported by the Centre for Economic Development, Transport and the Environment of North Karelia (project 1997), the Finnish Cultural Foundation North Karelia Regional fund (grant to VV) and the Academy of Finland (grant no. 133495 to OH).

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Authors and Affiliations

  1. Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101, Joensuu, Finland

    Virpi Virjamo, Riitta Julkunen-Tiitto & Eveliina Hiltunen

  2. Finnish Forest Research Institute, P.O. Box 18, FI-01301, Vantaa, Finland

    Heikki Henttonen

  3. Department of Biology, University of Eastern Finland, P.O. Box 1627, FI-70211, Kuopio, Finland

    Reijo Karjalainen

  4. Finnish Forest Research Institute, Juntintie 154, FI-77600, Suonenjoki, Finland

    Juhani Korhonen & Otso Huitu

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  1. Virpi Virjamo
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Correspondence to Virpi Virjamo.

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Virjamo, V., Julkunen-Tiitto, R., Henttonen, H. et al. Differences in Vole Preference, Secondary Chemistry and Nutrient Levels Between Naturally Regenerated and Planted Norway Spruce Seedlings. J Chem Ecol 39, 1322–1334 (2013). https://doi.org/10.1007/s10886-013-0352-6

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  • DOI: https://doi.org/10.1007/s10886-013-0352-6

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