Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Intra-annual wood density fluctuations and tree-ring width patterns are sex- and site-dependent in the dioecious conifer Juniperus thurifera L.


Key message

Sex and site conditions modulate intra- and inter-annual secondary growth and its climatic sensitivity in a dioecious Mediterranean conifer.


Divergent evolutionary pressures associated with differential reproductive costs in dioecious trees may lead to sex-related variation in non-reproductive functions. Sex-related differences may be site-dependent, with different outcomes depending on environmental conditions. We explored the effects of sex and environmental conditions on the climatic control of annual secondary growth and intra-annual wood density fluctuations (IADF) of a dioecious conifer (Juniperus thurifera L.) growing in two sites with contrasting hydrological conditions under a continental Mediterranean climate. Different sex-related strategies had variable effects on relative secondary growth, with females outperforming males under more favorable hydrological conditions, and males outperforming females under water-limited conditions. Ring width and IADF formation were driven by climatic factors occurring at different temporal scales. Tree-ring growth depended on factors acting prior to the initiation of the xylogenesis and to conditions directly affecting the duration and pace of cambial activity, and ring width, therefore, integrated a complex signal of factors occurring over a relatively long period, and on an annual cycle. In contrast, IADFs responded to singular short-term events that alleviated drought and promoted cambial reactivation during the summer arrest. Female trees showed a more opportunistic water use, displayed in the stronger ring-width response to June–July conditions. Enhanced cambial sensitivity in females set a lower threshold for IADF occurrence, leading to a higher frequency of IADFs irrespective of site. Intra-annual and inter-annual female growth patterns reflect an opportunistic strategy to benefit from favorable climatic windows.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Allen GA, Antos JA (1993) Sex ratio variation in the dioecious shrub Oemleria cerasiformis. Am Nat 141:537–553. doi:10.1086/285490

  2. Babst F, Bouriaud O, Papale D, Gielen B, Janssens IA, Nikinmaa E, Ibrom A, Wu J, Bernhofer C, Köstner B, Grünwald T, Seufert G, Ciais P, Frank D (2014) Above-ground woody carbon sequestration measured from tree rings is coherent with net ecosystem productivity at five eddy-covariance sites. New Phytol 201:1289–1303. doi:10.1111/nph.12589

  3. Bañuelos MJ, Obeso JR (2004) Resource allocation in the dioecious shrub Rhamnus alpinus: the hidden costs of reproduction. Evol Ecol Res 6:397–413

  4. Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2010) Cambial sensitivity to rising temperatures by natural condition and artificial heating from late winter to early spring in the evergreen conifer Cryptomeria japonica. Trees 24:43–52. doi:10.1007/s00468-009-0377-1

  5. Benavides R, Rabasa SG, Granda E, Escudero A, Hódar JA, Martínez-Vilalta J, Rincón AM, Zamora R, Valladares F (2013) Direct and indirect effects of climate on demography and early growth of Pinus sylvestris at the rear edge: changing roles of biotic and abiotic factors. PLoS One 8:e59824. doi:10.1371/journal.pone.0059824

  6. Bogino S, Bravo F (2009) Climate and intraannual density fluctuations in Pinus pinaster subsp. mesogeensis in Spanish woodlands. Can J For Res 39:1557–1565. doi:10.1139/X09-074

  7. Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol 185:471–480. doi:10.1111/j.1469-8137.2009.03073.x

  8. Camarero JJ, Rozas V, Olano JM (2014) Minimum wood density of Juniperus thurifera is a robust proxy of spring water availability in a continental Mediterranean climate. J Biogeogr 41:1105–1114. doi:10.1111/jbi.12271

  9. Campelo F, Nabais C, Freitas H, Gutiérrez E (2007) Climatic significance of tree-ring width and intra-annual density fluctuations in Pinus pinea from a dry Mediterranean area in Portugal. Ann For Sci 64:229–238. doi:10.1051/forest:2006107

  10. Campelo F, Vieira J, Nabais C (2013) Tree-ring growth and intra-annual density fluctuations of Pinus pinaster responses to climate: does size matter? Trees 27:763–777. doi:10.1007/s00468-012-0831-3

  11. Campelo F, Vieira J, Battipaglia G, de Luis M, Nabais C, Freitas H, Cherubini P (2015) Which matters most for the formation of intra-annual density fluctuations in Pinus pinaster: age or size? Trees 29:237–245. doi:10.1007/s00468-014-1108-9

  12. Cedro A, Iszkuło G (2011) Do females differ from males in European yew (Taxus baccata L.) in dendrochronological analysis? Tree Ring Res 67:3–11. doi:10.3959/2009-9.1

  13. Chen J, Duan B, Wang M, Korpelainen H, Li C (2014) Intra- and inter-sexual competition of Populus cathayana under different watering regimes. Funct Ecol 28:124–136. doi:10.1111/1365-2435.12180

  14. Cook ER, Holmes RL (1996) Guide for computer program ARSTAN. In: Grissino-Mayer HD, Holmes RL, Fritts HC (eds) The international tree ring data bank program library version 2.0 user’s manual. Tucson, AZ, USA: Laboratory of Tree-Ring Research, University of Arizona, pp 75-87

  15. Cook ER, Peters K (1981) The smoothing spline: a new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree Ring Bull 41:45–53

  16. Copenheaver CA, Pokorski EA, Currie JE, Abrams MD (2006) Causation of false ring formation in Pinus banksiana: a comparison of age, canopy class, climate and growth rate. For Ecol Manag 236:348–355. doi:10.1016/j.foreco.2006.09.020

  17. Cornelissen T, Stiling P (2005) Sex biased herbivory: a meta-analysis of effects of gender on plant-herbivore interactions. Oikos 111:488–500. doi:10.1111/j.1600-0706.2005.14075.x

  18. Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in box elder, Acer negundo. Ecology 74:798–815. doi:10.2307/1940807

  19. De Luis M, Novak K, Raventós J, Gričar J, Prislan P, Čufar K (2011) Climate factors promoting intra-annual density fluctuations in Aleppo pine (Pinus halepensis) from semiarid sites. Dendrochronologia 29:163–169. doi:10.1016/j.dendro.2011.01.005

  20. De Micco V, Battipaglia G, Brand WA, Linke P, Saurer M, Aronne G, Cherubini P (2012) Discrete versus continuous analysis of anatomical and delta C-13 variability in tree rings with intra-annual density fluctuations. Trees 26:513–524. doi:10.1007/s00468-011-0612-4

  21. DeSoto L, Camarero JJ, Olano JM, Rozas V (2012) Geographically structured and temporally unstable growth responses of Juniperus thurifera to recent climate variability in the Iberian Peninsula. Eur J For Res 131:905–917. doi:10.1007/s10342-011-0564-7

  22. Dudley LS, Galen C (2007) Stage-dependent patterns of drought tolerance and gas exchange vary between sexes in the alpine willow, Salix glauca. Oecologia 153:1–9. doi:10.1007/s00442-007-0712-4

  23. Edmondson JR (2010) The meteorological significance of false rings in eastern red cedar (Juniperus virginiana L.) from the southern great plains, USA. Tree Ring Res 66:19–33. doi:10.3959/2008-13.1

  24. El Mujtar VA, Perdomo MH, Gallo LA, Grau O (2012) Sex-related difference in susceptibility to cypress mortality in Austrocedrus chilensis from Northwestern Patagonia (Argentina). Bosque 33:221–226. doi:10.4067/S0717-92002012000200012

  25. Esteban R, Fernández-Marín B, Olano JM, Becerril JM, García-Plazaola JI (2014) Does plant colour matter? Wax accumulation as an indicator of decline in Juniperus thurifera. Tree Physiol 34:267–274. doi:10.1093/treephys/tpu006

  26. Gimeno TE, Camarero JJ, Granda E, Pias B, Valladares F (2012) Enhanced growth of Juniperus thurifera under a warmer climate is explained by a positive carbon gain under cold and drought. Tree Physiol 32:326–336. doi:10.1093/treephys/tps011

  27. Graff P, Rositano F, Aguiar MR (2013) Changes in sex ratios of a dioecious grass with grazing intensity: the interplay between gender traits, neighbour interactions and spatial patterns. J Ecol 101:1146–1157. doi:10.1111/1365-2745.12114

  28. Granda E, Camarero J, Gimeno T, Martínez-Fernández J, Valladares F (2013) Intensity and timing of warming and drought differentially affect growth patterns of co-occurring Mediterranean tree species. Eur J For Res 132:469–480. doi:10.1007/s10342-013-0687-0

  29. Grissino-Mayer HD (2001) Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree Ring Res 57:205–221

  30. Hughes MK, Swetnam TW, Diaz HF (2011) Dendroclimatology: progress and prospects. Springer Verlag, Berlin 365 pp

  31. Hultine KR, Bush SE, West AG, Burtch KG, Pataki DE, Ehleringer JR (2008) Gender specific patterns of above ground allocation, and water use in a dominant riparian tree species: box elder (Acer negundo). Tree Physiol 28:1383–1394. doi:10.1093/treephys/28.9.1383

  32. Hultine KR, Burtch KG, Ehleringer JR (2013) Gender specific patterns of carbon uptake and water use in a dominant riparian tree species exposed to a warming climate. Glob Chang Biol 19:3390–3405. doi:10.1111/gcb.12230

  33. Iszkuło G, Boratyński A (2011) Initial period of sexual maturity determines the greater growth rate of male over female in the dioecious tree Juniperus communis subsp. communis. Acta Oecol 37:99–102. doi:10.1016/j.actao.2011.01.001

  34. Iszkuło G, Jasińska AK, Romo A, Tomaszewski D, Szmyt J (2011) The greater growth rate of male over female of the dioecious tree Juniperus thurifera only in worse habitat conditions. Dendrobiology 66:15–24

  35. Kramer PJ (1964) The role of water in wood formation. In: Zimmermann MH (ed) The formation of wood in forest trees. Academic Press, New York, pp 519–532

  36. Kurczynska EU, Dmuchowski W, Wloch W, Bytnerowicz A (1997) The influence of air pollutants on needles and stems of Scots pine (Pinus sylvestris L.) trees. Env Poll 98:325–334. doi:10.1016/S0269-7491(97)00141-3

  37. Li X, Liang E, Gričar J, Prislan P, Rossi S, Čufar K (2012) Age dependence of xylogenesis and its climatic sensitivity in Smith fir on the south-eastern Tibetan Plateau. Tree Physiol 33:48–56. doi:10.1093/treephys/tps113

  38. Lupi C, Morin H, Deslauriers A, Rossi S (2010) Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant Cell Environ 33:1721–1730. doi:10.1111/j.1365-3040.2010.02176.x

  39. Mezquida ET, Olano JM (2013) What makes a good neighborhood? Temporal and spatial variation in pre-dispersal fruit predation in the Spanish juniper. Oecologia 173:483–492. doi:10.1007/s00442-013-2631-x

  40. Montesinos D, De Luis M, Verdú M, Raventos J, Garcia-Fayos P (2006) When, how and how much: gender-specific resource-use strategies in the dioecious tree Juniperus thurifera. Ann Bot 98:885–889. doi:10.1093/aob/mcl172

  41. Montesinos D, García-Fayos P, Verdú M (2012a) Genders in Juniperus thurifera have different functional responses to variations in nutrient availability. New Phytol 193:705–712. doi:10.1111/j.1469-8137.2011.03982.x

  42. Montesinos D, García-Fayos P, Verdú M (2012b) Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree. Oikos 118:529–538. doi:10.1111/j.1600-0706.2011.20399.x

  43. Novak N, Saz MA, Čufar K, Raventós J, De Luis M (2013) Age, climate and intra-annual density fluctuations in Pinus halepensis in Spain. IAWA J 34:459–474. doi:10.1163/22941932-00000037

  44. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348. doi:10.1046/j.1469-8137.2002.00477.x

  45. Olano JM, Eugenio M, Escudero A (2011) Site effect is stronger than species identity in driving demographic responses of Helianthemum shrubs in gypsum environments. Am J Bot 90:1–8. doi:10.3732/ajb.1000505

  46. Olano JM, Eugenio M, García-Cervigón AI, Folch M, Rozas V (2012) Quantitative tracheid anatomy reveals a complex environmental control of wood structure in continental Mediterranean climate. Int J Plant Sci 173:137–149. doi:10.1086/663165

  47. Olano JM, Arzac A, García-Cervigón A, von Arx G, Rozas V (2013) New star on the stage: amount of ray parenchyma in tree rings shows a link to climate. New Phytol 198:486–495. doi:10.1111/nph.12113

  48. Olano JM, Linares JC, García-Cervigón AI, Arzac A, Delgado A, Rozas V (2014) Drought-induced increase in water-use efficiency reduces secondary tree growth and tracheid wall thickness in a Mediterranean conifer. Oecologia 176:273–283. doi:10.1007/s00442-014-2989-4

  49. Olivar J, Bogino S, Spiecker H, Bravo F (2012) Climate impact on growth dynamics and intra-annual density fluctuations in Aleppo pine (Pinus halepensis) tree on different crown classes. Dendrochronologia 30:35–47. doi:10.1016/j.dendro.2011.06.001

  50. Pasho E, Camarero JJ, de Luis M, Vicente-Serrano SM (2011) Impacts of drought at different time scales on forest growth across a wide climatic gradient in north-eastern Spain. Agric For Meteorol 151:1800–1811. doi:10.1016/j.agrformet.2011.07.018

  51. Priya AB, Bhat KM (1997) Wood anatomical changes in juvenile teak due to insect defoliation. IAWA J 18:311–317. doi:10.1163/22941932-90001496

  52. Rawson HM, Begg JE, Woodward RG (1977) The effect of atmospheric humidity on photosynthesis, transpiration and water use efficiency of leaves of several plant species. Planta 134:5–10. doi:10.1007/BF00390086

  53. Retuerto R, Fernández Lema B, Rodríguez Roiloa S, Obeso JR (2000) Gender, light and water effects in carbon isotope discrimination, and growth rates in the dioecious tree Ilex aquifolium. Funct Ecol 14:529–537. doi:10.1046/j.1365-2435.2000.t01-1-00454.x

  54. Rigling A, Waldner PO, Forster T, Bräker OU, Pouttu A (2001) Ecological interpretation of tree-ring width and intraannual density fluctuations in Pinus sylvestris on dry sites in the central Alps and Siberia. Can J For Res 31:18–31. doi:10.1139/x00-126

  55. Rossi S, Girard M-J, Morin H (2014) Lengthening of the duration of xylogenesis engenders disproportionate increases in xylem production. Glob Chang Biol 20:2261–2271. doi:10.1111/gcb.12470

  56. Rozas V, Olano JM (2012) Environmental heterogeneity and neighbourhood interference modulate the individual response of Juniperus thurifera tree-ring growth to climate. Dendrochronologia 31:105–113. doi:10.1016/j.dendro.2012.09.001

  57. Rozas V, DeSoto L, Olano JM (2009) Sex-specific, age-dependent sensitivity of tree-ring growth to climate in the dioecious tree Juniperus thurifera. New Phytol 182:687–697. doi:10.1111/j.1469-8137.2009.02770.x

  58. Rozas V, García-González I, Zas R (2011) Climatic control of intra-annual wood density fluctuations of Pinus pinaster in NW Spain. Trees 25:443–453. doi:10.1007/s00468-010-0519-5

  59. Vieira J, Campelo F, Nabais C (2009) Age-dependent responses of tree-ring growth and intra-annual density fluctuations of Pinus pinaster to Mediterranean climate. Trees 23:257–265. doi:10.1007/s00468-008-0273-0

  60. Vilas JS, Pannell JR (2011) Sexual dimorphism in resource acquisition and deployment: both size and timing matter. Ann Bot 107:119–126. doi:10.1093/aob/mcq209

  61. Willson CJ, Manos PS, Jackson RB (2008) Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae). Am J Bot 95:299–314. doi:10.3732/ajb.95.3.299

  62. Wimmer R, Strumia G, Holawe F (2000) Use of false rings in Austrian pine to reconstruct early growing season precipitation. Can J For Res 30:1691–1697. doi:10.1139/cjfr-30-11-1691

  63. Xu X, Yang F, Xiao X, Zhang S, Korpelainen H, Li C (2008) Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant Cell Environ 31:850–860. doi:10.1111/j.1365-3040.2008.01799.x

  64. Young PJ, Megonigal JP, Sharitz RR, Day FP (1993) False ring formation in baldcypress (Taxodium distichum) saplings under two flooding regimes. Wetlands 13:293–298. doi:10.1007/BF03161295

Download references

Author contribution statement

AA, AIGC and JMO designed and executed the sampling. JMO and AIGC analyzed the data. JMO wrote the first draft that was worked during several rounds with VR, AIGC and AA.


We are especially grateful to Gonzalo Juste for his invaluable labor with laboratory tasks and chronologies development. Sergio Vicente provided access and assessment about best climatic data available. We thank David Brown for English language advice. This work was supported by a FPI-EHU grant to A. A., a FPI-MICINN grant to A. I. G.-C. and project CGL2012-34209 (Spanish Ministry of Economy and Competitivity).

Conflict of interest

Authors acknowledge no conflict of interests.

Author information

Correspondence to José Miguel Olano.

Additional information

Communicated by Y. Sano.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Olano, J.M., García-Cervigón, A.I., Arzac, A. et al. Intra-annual wood density fluctuations and tree-ring width patterns are sex- and site-dependent in the dioecious conifer Juniperus thurifera L.. Trees 29, 1341–1353 (2015). https://doi.org/10.1007/s00468-015-1212-5

Download citation


  • Dendroecology
  • Dioecy
  • IADF
  • Juniperus thurifera
  • Mediterranean climate