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

Journal of Chemical Ecology

Volumn 39, Issue 10, 2013, Pages 1322-1334

  Virjamo, Virpi ^a   Julkunen Tiitto, Riitta ^a   Henttonen, Heikki ^b   Hiltunen, Eveliina ^a   Karjalainen, Reijo ^a   Korhonen, Juhani ^b   Huitu, Otso ^b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

Author keywords

Herbivory; Microtus agrestis; Nitrogen; Phenolics; Picea abies; Piperidine alkaloids

Indexed keywords

ALKALOID; FOOD PREFERENCE; HERBIVORY; NITROGEN; PHENOLIC COMPOUND; PLANT-HERBIVORE INTERACTION; SEEDLING;

FENNOSCANDIA;

ALKALOID; NITROGEN; PHENOL DERIVATIVE;

ANIMAL; ARTICLE; ARVICOLINAE; COMPARATIVE STUDY; FOOD PREFERENCE; METABOLISM; PHYSIOLOGY; REGENERATION; SEASON; SEEDLING; SPRUCE;

ALKALOIDS; ANIMALS; ARVICOLINAE; FOOD PREFERENCES; NITROGEN; PHENOLS; PICEA; REGENERATION; SEASONS; SEEDLING;

EID: 84886745671     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-013-0352-6     Document Type: Article

References (53)

1. Baxter R, Hansson L (2001) Bark consumption by small rodents in the northern and southern hemispheres. Mammal Rev 31: 47-59.
2. 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.
3. 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.
4. 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.
5. Clausen TP, Reichardt PB, Bryant JP (1986) Pinosylvin and pinosylvin methyl ether as feeding deterrents in green alder. J Chem Ecol 12: 2117-2131.
6. 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.
7. 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.
8. 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.
9. 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.
10. Gerson EA, Kelsey RG (1999a) Piperidine alkaloids in nitrogen fertilized Pinus ponderosa. J Chem Ecol 25: 2027-2039.
11. 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.
12. 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.
13. Gerson EA, Kelsey RG (2004) Piperidine alkaloids in North American Pinus taxa: implications for chemosystematics. Biochem Syst Ecol 32: 62-74.
14. 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.
15. Gill RMA (1992) A Review of damage by mammals in north temperate forest. 2. Small Mammals. Forestry 65: 281-308.
16. Hagerman AE (2002) The tannin handbook. (updated: 2011). Department of Chemistry & Biochemistry, Miami University, Oxford, OH 45056. http://www. users. muohio. edu/hagermae/.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. Hjältén J, Palo T (1992) Selection of deciduous trees by free ranging voles and hares in relation to plant chemistry. Oikos 63: 477-484.
23. Hjältén J, Danell K, Ericson L (2004) Hare and vole browsing preferences during winter. Acta Theriol 49: 53-62.
24. Hodson MJ, Sangster AG (1999) Aluminium/silicon interactions in conifers. J Inorg Biochem 76: 89-98.
25. 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.
26. Julkunen-Tiitto R, Sorsa S (2001) Testing the effects of drying methods on willow flavonoids, tannin and salicylates. J Chem Ecol 27: 779-789.
27. 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.
28. Marquis RJ, Batzli GO (1989) Influence of chemical factors on palatability of forage to voles. J Mamm 79: 503-511.
29. Massey FP, Ennos AR, Hartley SE (2007) Grasses and the resource availability hypothesis: the importance of silica-based defences. J Ecol 95: 414-424.
30. 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.
31. Massey FP, Smith MJ, Lambin X, Hartley SE (2008) Are silica defences in grasses driving vole population cycles? Biol Lett 4: 419-422.
32. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Syst 11: 119-161.
33. Nilsson U, Luoranen J, Kolström T, Örlander G, Puttonen P (2010) Reforestation with planting in northern Europe. Scand J For Res 25: 283-294.
34. 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.
35. 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.
36. Pan H, Lundgren L (1985) Phenolic extractives from root bark of Picea abies. Phytochemistry 39: 1423-1428.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. Schneider MJ, Montali JA, Hazen D, Stanton CE (1991) Alkaloids of Picea. J Nat Prod 54: 905-909.
43. Solhaug KA (1990) Stilbene glucosides in bark and needles from Picea species. Scand J For Res 5: 59-67.
44. 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.
45. Stermitz FR, Kamm CD, Tawara JN (2000) Piperidine alkaloids of spruce (Picea) and fir (Abies) species. Biochem Syst Ecol 28: 177-181.
46. 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.
47. 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.
48. 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.
49. 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.
50. Todd FG, Stermitz FR, Blokhin AV (1995) Piperidine alkaloid content of Picea pungens (Colorado blue spruce). Phytochemistry 40: 401-406.
51. 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.
52. Wink M, Meissner C, Witte L (1995) Patterns of quinolizidine alkaloids in 56 species of the genus Lupinus. Phytochemistry 38: 139-153.
53. 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.