Abstract
Dieback of the terminal shoot and consequently bushy growth induced by boron deficiency have been reported widely throughout the world in several tree species. Recently, similar growth damage was documented in half of the young spruce stands in eastern Finland. To clarify the role of B deficiency, the light microscopic structure of emerging buds and of developing and previous-year needles of mature Norway spruce (Picea abies L. Karst.) from damaged (D stand), partly damaged (PD stand) and healthy (H stand) stands were analysed. The samples, on which needle nutrient concentrations were also determined, were taken seven times between early spring (April) and early winter (November). Cell death characterized by precipitation of the cell content, possibly due to the release of tannins after membrane rupture, was seen in the apex of emerging buds, and this led to fatal damage in about half of the buds in the trees from the D stand, where the needle B concentration was well below the deficiency level of 4–5 mg kg−1. Furthermore, an increase in living cells that accumulated tannins in the vacuoles, which is a common stress and/or defense reaction, was found in the primordial shoots of buds and in the differentiating needles in the PD and D stands. The increase in the areas of the central cylinder and of the xylem found in the needles indicate structural plasticity during needle differentiation to drought. The time frame for bud emergence from late May up to mid-September means that an adequate B supply is necessary throughout the summer in order to avoid fatal bud damage and thus bushy growth of the trees.
Similar content being viewed by others
References
Anglberger H, Sieghardt M, Katzensteiner K, Halmschlager E (2003) Needle nutrient status of Sirococcus shoot blight-diseased and healthy Norway spruces. For Path 33:21–29
Aronsson A (1983) Growth disturbances caused by boron deficiency in some fertilized pine and spruce stands on mineral soils. Commun Inst For Fenn 116:116–122
Bílková J, Albrechtová J, Opatrná J (1999) Histochemical detection and image analysis of non-specific esterase activity and the amount of polyphenols during annual bud development in Norway spruce. J Exp Bot 35:1129–1138
Braekke FH (1983) Occurrence of growth disturbance problems in Norwegian and Swedish forestry. Commun Inst For Fenn 116:20–25
Braekke FH (1994) Diagnostiske grenseverdier for naeringselementer i gran- og furunåler. Aktuelt fra Skogforsk 15:11 (In Norwegian)
Cajander AK (1949) Forest types and their significance. Acta Forestalia Fennica 56:69
Cakmak I, Kurz H, Marschner H (1995) Short-term effects of boron, germanium, and high light intensity on membrane permeability in boron deficient leaves of sunflower. Physiol Plant 95:11–18
Cakmak I, Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193:71–83
Cannel MGR, Willet SC (1975) Rates and times at which needles are initiated in buds on differing provenances of Pinus contorta and Picea sitchensis in Scotland. Can J For Res 5:367–380
Carter RE Brockley RP (1990) Boron deficiencies in British Columbia: diagnosis and treatment evaluation. For Ecol Manage 37:83–94
Correia MJ, Coelho D, David MM (2001) Response to seasonal drought in three cultivars of Ceratonia siliqua: leaf growth and water relations. Tree Physiol 21:645–653
de Faÿ E, Vacher V, Humbert F (2000) Water-related phenomena in winter buds and twigs of Picea abies L. (Karst.) until bud-burst: a biological, histological and NMR study. Ann Bot 86:1097–1107
Dell B, Huang L (1997) Physiological response of plants to low boron. Plant Soil 193:103–120
Deslauriers A, Morin H (2005) Intra-annual tracheid production in balsam fir stem and the effect of meteorological variables. Trees 19:402–408
Dordas C, Brown PH (2005) Boron deficiency affects cell viability, phenolic leakage and oxidative burst in rose cell cultures. Plant Soil 268:293–301
Fink S (1999) Pathological and regenerative plant anatomy. Berlin: Gebruder Bornträger
Gilmore DW, Seymour RS, Halteman WA, Greenwood MS (1995) Canopy dynamics and the morphological development of Abies balsamea: effects of foliage age on specific leaf area and secondary vascular development. Tree Physiol 15:47–55
Goldberg S (1997) Reactions of boron with soils. Plant Soil 193:35–48
Halmschlager E, Gabler A, Andrae F (2000) The impact of Sirococcus shoot blight on radial and height growth of Norway spruce (Picea abies) in young plantations. For Path 30:127–133
Halonen O, Tulkki H, Derome J (1983) Nutrient analysis methods. Metsäntutkimuslaitoksen tiedonantoja 121:28
Heikinheimo O (1915) Kaskiviljelyksen vaikutus Suomen metsiin. Acta Forestalia Fennica 4(2):264
Holopainen T, Anttonen S, Wulff A, Palomäki V, Kärenlampi L (1992) Comparative evaluation of the effects of gaseous pollutants, acidic deposition and mineral deficiencies: structural changes in the cells of forest plants. Agric Ecosyst Environ 42:365–398
Jäntti A (1947) Suomen laidunolot. Referat: Die Weideverhältnisse in Finnland. Acta Forestalia Fennica 53:254
Järvinen E, Hokkanen TJ, Kuuluvainen T (1993) Spatial heterogeneity and relationships of mineral soil properties in boreal Pinys sylvestris stand. Scand J For Res 8:435–445
Jokela A, Bäck J, Huttunen S, Jalkanen R (1995) Excess nitrogen fertilization and the structure of Scots-pine needles. Eur J For Path 25:109–124
Jukka L (1988) Metsänterveysopas. Metsätuhot ja niiden torjunta. Samreka Oy, Helsinki, 168 p
Liakopoulos G, Karabourniotis G (2005) Boron deficiency and concentrations and composition of phenolic compounds in Olea europaea leaves: a combined growth chamber and field study. Tree Physiol 25:307–315
Lilja S (1967) Tuomen merkityksestä kuusen tuomiruostesienen, Pucciniastrum padi (Kunze & Schum.) Diet. esiintymiselle kuusessa. Summary: On the occurrence of the bird cherie (Prunus padus L.) for the occurrence of the rust Puccniastrum padi (Kunze & Schum.) Diet. in spruce. Silva Fennica 1:45–62
Linder S (1995) Foliar analysis for detecting and correcting nutrient imbalances in Norway spruce. Ecol Bull (Copenhagen) 44:178–190
Loomis WD, Durst RW (1992) Chemistry and biology of boron. BioFactors 3:229–239
Matoh T (1997) Boron in plant cell walls. Plant Soil 193:59–70
Möttönen M, Järvinen E, Hokkanen TJ, Kuuluvainen T, Ohtonen R (1999) Spatial distribution of soil ergosterol in the organic layer of a mature Scots pine (Pinus sylvestris L.) forest. Soil Biol Biochem 31:503–516
Möttonen M, Lehto T, Aphalo PJ (2001) Growth dynamics and mycorrhizas of Norway spruce (Picea abies) seedlings in relation to boron supply. Trees 15:319–326
Power PP, Woods WG (1997) The chemistry of boron and its specification in plants. Plant Soil 193:1–13
Raitio H (1983) Macro- and microscopic symptoms in growth disturbed forest trees. Commun Inst For Fenn 116:35–39
Raitio H, Merilä P (1998) Seasonal variation in the size and chemical composition of Scots pine and Norway spruce needles in different conditions. Technical Report, European Programme for the Intensive Monitoring of Forest Ecosystems/Level II, Finland, The Finnish Forest Research Institute, Parkano Research Station, 44 p.
Raulo J, Leikola M (1974) Tutkimuksia puiden vuotuisen pituuskasvun ajoittumisesta. Summary: Studies on the annual height growth of trees. Commun Inst For Fenn 81(2):19
Rehfuess K-E, Bosch C, Pfannkuch E (1983) Nutrient imbalances in coniferous stands in southern Germany. Commun Inst For Fenn 116:122–130
Rerkasem B, Jamjod S (1997) Genotypic variation in plant response to low boron and implications for plant breeding. Plant Soil 193:169–180
Richardson AD, Ashton PMS, Berlyn GP, Mcgroddy ME, Cameron IR (2001) Within-crown foliar plasticity of western hemlock, Tsuga heterophylla, in relation to stand age. Ann Bot 88:1007–1015
Ryyppö A, Sutinen S, Mäenpää M, Vapaavuori E, Repo T (1997) Frost damage and recovery of Scots pine seedlings at the end of the growing season. Can J For Res 27:1376–1382
Saalas U (1949) Suomen metsähyönteiset sekä muut metsälle vahingolliset ja hyödylliset eläimet. Suomelainen tiedeakatemia. Suomen tiedettä no 5, WSOY, Helsinki, 719 p (In Finnish)
Saarsalmi A, Tamminen P (2005) Boron, phosphorus and nitrogen fertilization in Norway spruce stands suffering from growth disturbances. Silva Fennica 39(3):351–364
Silfverberg K (1980) Kuusen kasvuhäiriö ja hivenravinteet. Abstract: Micronutrional disorder in Norway spruce. Folia For 432:13
Soikkeli S (1980) Ultrastructure of the mesophyll in Scots pine and Norway spruce: seasonal variation and molarity of fixative buffer. Protoplasma 103:241–252
Stavrianakou S, Liakopoulos G, Karabourniotis G (2006) Boron deficiency on growth, photosynthesis and relative concentrations of phenolics of Dittrichia viscose (Asteraceae). Environ Exp Bot 56:293–300
Stone EL (1990) Boron deficiency and excess in forest trees: a review. For Ecol Manage 37:49–75
Sutinen S, Koivisto L (1995) Microscopic structure of conifer needles as a diagnostic tool in the field. In: Munawar M, Hänninen O, Roy S, Munawar N, Kärenlampi L, Brown D (eds) Bioindicators of environmental health. Ecovision world monograph series. SPB Academic Publishing, Amsterdam, The Netherlands, pp 73–81
Svobodová H, Lipavská H, Albrechtová J (2000) Non-structural carbohydrate status in Norway spruce buds in the context of annual bud structural development as affected by acidic pollution. Environ Exp Bot 43:253–265
Tamminen P (1991) Kangasmaan ravinnetunnusten ilmaiseminen ja viljavuuden alueellinen vaihtelu Etelä-Suomessa. Summary: Expression of soil nutrient status and regional variation in soil fertility of forested sites in southern Finland, FF 777, 40 p
Tamminen P, Saarsalmi A (2004) Viljavien maiden nuorten kuusikoiden neulasten booripitoisuus Etelä-Suomessa. Metsätieteen aikakauskirja 3/2004:271–283 (In Finnish)
Wikner B (1983) Distribution and mobility of boron in forest ecosystems. Commun Inst For Fenn 116:131–141
Acknowledgements
We thank Marja-Leena Jalkanen, Osmo Korhonen and Seija Repo for their assistance in the field and in the laboratory.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Rennenberg
Rights and permissions
About this article
Cite this article
Sutinen, S., Vuorinen, M. & Rikala, R. Developmental disorders in buds and needles of mature Norway spruce, Picea abies (L.) Karst., in relation to needle boron concentrations. Trees 20, 559–570 (2006). https://doi.org/10.1007/s00468-006-0071-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-006-0071-5