Journal of Plant Research

, Volume 131, Issue 2, pp 261–269 | Cite as

Cessation of annual apical growth and partial death of cambium in stem of Abies sachalinensis under intensive shading

  • Yuko Yasuda
  • Yasuhiro Utsumi
  • Naoaki Tashiro
  • Shinya Koga
  • Kenji Fukuda
Regular Paper


This study evaluated variation in the height at which absent rings and internodes were detected along stem of Abies sachalinensis trees grown under shade for 39 years. Eight sample trees planted in 1974 under a secondary forest in Japan were felled in 2013 and analyzed. A. sachalinensis is a monopodial species in which it is possible to measure annual apical growth using the distinct internodes. We applied microscopic analysis on 154 stem disks from the stem base to the top to evaluate the cessation of apical and radial growth caused by intensive shading. Cessation of apical stem growth for one or more years was found in 6 out of 8 sample trees. We termed this phenomenon as “absent internode”. In addition, the absent growth rings were detected more frequently in the lower part of sample stems, and the number of absent rings at the stem base did not correspond with the number of absent internodes in the six trees. From cellular level observation, the five suppressed trees had no living cambial cells at the stem base but had living cells at the stem top. The cessation of the apical and radial growth did not occur synchronously but did occur independently under a shade environment in A. sachalinensis.


Internode Absent ring Cambium Monopodial species Shade environment 



The authors thank Kazuta Takahashi and technical staff of Shiiba Research Forest, Kyushu University for supporting sample collections. The authors also thank Eiko Megan Uchida and member of Laboratory of Forest Production Control, Kyushu University Forest, for valuable comments on our manuscript. This study was supported in part by JSPS KAKENHI (Nos. 26450233 and 15H02450).


  1. Abe H, Nakai T (1999) Effect of the water status within a tree on tracheid morphogenesis in Cryptomeria japonica D. Don. Trees 14:124–129Google Scholar
  2. Abe H, Nakai T, Utsumi Y, Kagawa A (2003) Temporal water deficit and wood formation in Cryptomeria japonica. Tree Physiol 23:859–863CrossRefPubMedGoogle Scholar
  3. Barbosa ACF, Pace MR, Witovisk L, Angyalossy V (2010) A new method to obtain good anatomical slides of heterogeneous plant parts. IAWA J 31:373–383Google Scholar
  4. Bormann FH (1965) Changes in the growth pattern of white pine trees undergoing suppression. Ecology 46:269–277CrossRefGoogle Scholar
  5. Claveau Y, Messier C, Comeau PG, Coates KD (2002) Growth and crown morphological responses of boreal conifer seedlings and saplings with contrasting shade tolerance to a gradient of light and height. Can J For Res 32:458–468CrossRefGoogle Scholar
  6. Dlugos DM, Collins H, Bartelme EM, Drenovsky RE (2015) The non-native plant Rosa multiflora expresses shade avoidance traits under low light availability. Am J Bot 102:1323–1331CrossRefPubMedGoogle Scholar
  7. Duchesneau R, Lesage I, Messier C, Morin H (2001) Effects of light and intraspecific competition on growth and crown morphology of two size classes of understory balsam fir saplings. For Ecol Manage 140:215–225CrossRefGoogle Scholar
  8. Eilmann B, Zweifel R, Buchmann N et al (2011) Drought alters timing, quantity, and quality of wood formation in Scots pine. J Exp Bot 62:2763–2771CrossRefPubMedGoogle Scholar
  9. Eklund L, Little CH a, Riding RT (1998) Concentrations of oxygen and indole-3-acetic acid in the cambial region during latewood formation and dormancy development in Picea abies stems. J Exp Bot 49:205–211Google Scholar
  10. Ferreira BG, Teixeira CT, Isaias RMS (2014) Efficiency of the polyethylene-glycol (PEG) embedding medium for plant histochemistry. J Hisochem Cytochem 62:1–7Google Scholar
  11. Fritts HC (1976) Tree ring and climate, 2nd edn. The Blackburn Press, CaldwellGoogle Scholar
  12. Gebauer R, Volařík D, Urban J et al (2012) Effects of different light conditions on the xylem structure of Norway spruce needles. Trees 26:1079–1089CrossRefGoogle Scholar
  13. George SS, Ault TR, Torbenson MCA (2013) The rarity of absent growth rings in Northern Hemisphere forests outside the American Southwest. Geophys Res Lett 40:3727–3731CrossRefGoogle Scholar
  14. Hiura T, Sano J, Konno Y (1996) Age strucuture and response to fine-scale disturbances of Abies sachalinensis, Picea jezoensis, Picea glehnii, and Betula ermanii growing under the influence of a dwarf bamboo understory in northern Japan. Can J For Res 26:289–297CrossRefGoogle Scholar
  15. Kerhoulas LP, Kane JM (2012) Sensitivity of ring growth and carbon allocation to climatic variation vary within ponderosa pine trees. Tree Physiol 32:14–23CrossRefPubMedGoogle Scholar
  16. Kienholz R (1934) Leader, needle, cambial, and root growth of certain conifers and their interrelations. Bot Gaz 96(1):73–92CrossRefGoogle Scholar
  17. King DA (1997) Branch growth and biomass allocation in Abies amabilis saplings in contrasting light environments. Tree Physiol 17:251–258CrossRefPubMedGoogle Scholar
  18. Kohyama T (1980) Growth pattern of Abies mariesii saplings under conditions of open-growth and suppression. Bot Mag Tokyo 93:13–24CrossRefGoogle Scholar
  19. Kohyama T (1984) Regeneration and coexistence of two Abies species dominating subalpine forests in central Japan. Oecologia 62:156–161CrossRefPubMedGoogle Scholar
  20. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488CrossRefGoogle Scholar
  21. Kozlowski TT, Pallardy SG (1997) Physiology of woody plants, Second. Academic Press, San DiegoGoogle Scholar
  22. Kramer PJ, Kozlowski TT (1979) Physiology of woody plants. Academic Press, New YorkGoogle Scholar
  23. Lorimer CG, Dahir SE, Singer MT (1999) Frequency of partial and missing rings in Acer saccharum in relation to canopy position and growth rate. Plant Ecol 143:189–202CrossRefGoogle Scholar
  24. Lorimer CG, Dahir SE, Nordheim EV (2001) Tree mortality rates and longevity in mature and old-growth hemlock-hardwood forests. J Ecol 89:960–971CrossRefGoogle Scholar
  25. Maguire DA, Benett WS (1996) Patterns in vertical distribution of foliage in young coastal Douglas-fir. Can J For Res 26:1991–2005CrossRefGoogle Scholar
  26. Mencuccini M (2002) Hydraulic constraints in the functional scaling of trees. Tree Physiol 22:553–565CrossRefPubMedGoogle Scholar
  27. Naidu SL, Delucia EH (1997) Growth, allocation and water relations of shade-grown Quercus rubra L. saplings exposed to a late-season canopy gap. Ann Bot 80:335–344CrossRefGoogle Scholar
  28. Naidu SL, Delucia EH (1998) Physiological and morphological acclimation of shade grown tree seedlings to late season canopy gap formation. Plant Ecol 138:27–40CrossRefGoogle Scholar
  29. Niklasson M (2002) A comparison of three age determination methods for suppressed Norway spruce: implications for age structure analysis. For Ecol Manage 161:279–288CrossRefGoogle Scholar
  30. O’Connell BM, Kelty MJ (1994) Crown architecture of understory and open-grown white pine (Pinus strobus L.) saplings. Tree Physiol 14:89–102CrossRefPubMedGoogle Scholar
  31. Oribe Y, Funada R, Kubo T (2003) Relationships between cambial activity, cell differentiation and the localization of starch in storage tissues around the cambium in locally heated stems of Abies sachalinensis. (Schmidt) Masters Trees 17:185–192Google Scholar
  32. Petritan AM, von Lüpke B, Petritan IC (2009) Influence of light availability on growth, leaf morphology and plant architecture of beech (Fagus sylvatica L.), maple (Acer pseudoplatanus L.) and ash (Fraxinus excelsior L.) saplings. Eur J For Res 128:61–74CrossRefGoogle Scholar
  33. Rigling A, Bräker O, Schneiter G, Schweingruber F (2002) Intra-annual tree-ring parameters indicating differences in drought stress of Pinus sylvestris forests within the Erico-Pinion in the Valais (Switzerland). Plant Ecol 163:105–121CrossRefGoogle Scholar
  34. Rossi S, Simard S, Rathgeber CBK et al (2009) Effects of a 20-day-long dry period on cambial and apical meristem growth in Abies balsamea seedlings. Trees 23:85–93CrossRefGoogle Scholar
  35. Schoonmaker AL, Hacke UG, LandhäUsser SM et al (2010) Hydraulic acclimation to shading in boreal conifers of varying shade tolerance. Plant Cell Environ 33:382–393CrossRefPubMedGoogle Scholar
  36. Schulte PJ (2012) Vertical and radial profiles in tracheid characteristics along the trunk of Douglas-fir trees with implications for water transport. Trees 26:421–433CrossRefGoogle Scholar
  37. Schweingruber FH, Börner A, Schulze E-D (2006) Atlas of woody plant stems: evolution, structure, and environmental modifications. Springer, BerlinGoogle Scholar
  38. Sellin A (1993) Resistance to water flow in xylem of Picea abies (L.) Karst. trees grown under contrasting light conditions. Trees 7:220–226CrossRefGoogle Scholar
  39. Sprugel DG (2002) When branch autonomy fails: Milton’s Law of resource availability and allocation. Tree Physiol 22:1119–1124CrossRefPubMedGoogle Scholar
  40. Stockfors J, Linder S (1998) Effect of nitrogen on the seasonal course of growth and maintenance respiration in stems of Norway spruce trees. Tree Physiol 18:155–166CrossRefPubMedGoogle Scholar
  41. Suzuki E, Ota K, Igarashi T, Fujiwara K (1987) Regeneration process of coniferous forests in northern Hokkaido I. Abies sachalinensis forest and Picea glehnii forest. Ecol Res 2:61–75CrossRefGoogle Scholar
  42. Takahashi K, Obata Y (2014) Growth, allometry and shade tolerance of understory saplings of four subalpine conifers in central Japan. J Plant Res 127:329–338CrossRefPubMedGoogle Scholar
  43. Takaoka S (1993) The effect of missing rings on stand-age estimation of even-aged forests in northern Hokkaido, Japan. Ecol Res 8:341–347CrossRefGoogle Scholar
  44. Thomas PA (2000) Trees: Their natural history. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  45. Tucker GF, Hinckley TM, Leverenz J, Jiang S (1987) Adjustments of foliar morphology in the acclimation of understory Pacific silver fir following clearcutting. For Ecol Manage 21:249–268CrossRefGoogle Scholar
  46. Turberville HW, Hough AF (1939) Errors in age counts of suppressed trees. J For 37:417–418Google Scholar
  47. Waring KM, O’Hara KL (2006) Estimating relative error in growth ring analyses of second-growth coast redwood (Sequoia sempervirens). Can J For Res 36:2216–2222CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  • Yuko Yasuda
    • 1
  • Yasuhiro Utsumi
    • 2
  • Naoaki Tashiro
    • 2
  • Shinya Koga
    • 2
  • Kenji Fukuda
    • 3
  1. 1.Graduate School of Bioresource and Bioenvironmental SciencesKyushu UniversityFukuokaJapan
  2. 2.Graduate school of AgricultureKyushu UniversityFukuokaJapan
  3. 3.Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan

Personalised recommendations