Plant Ecology and Evolution 154(3): 321-331, doi: 10.5091/plecevo.2021.1793
30-year cone production dynamics in Siberian stone pine (Pinus sibirica) in the southern boreal zone: a causal interpretation
expand article infoSergey Goroshkevich, Svetlana Velisevich, Aleksandr Popov, Oleg Khutornoy, Galina Vasilyeva
‡ Institute of Monitoring of Climatic and Ecological Systems, Siberian Branch of the Russian Academy of Sciences, Tomsk, Russia
Open Access
Abstract

Background and aims – Siberian stone pine is a keystone species for Siberia, and numerous studies have analyzed Siberian stone pine seeding dynamics in connection with the dynamics of weather conditions. However, all studies were based on observations before 1990. The aim of the study was to expand our knowledge about the balance of weather and climatic factors in the regulation of cone production to enable conclusions about the current reproductive function in Siberian stone pine.

Material and methods – We monitored Siberian stone pine cone production in the southeastern region of the Western Siberian Plain, in association with climatic factors, over a period of 30 years. To analyze the relationship with weather conditions, we used the trait mature cone number per tree and weather data obtained from the weather station in Tomsk.

Key results – During this period, cone production decreased by about one-third, mainly caused by the complete absence of high yields. The main factor negatively affecting cone production was late spring frost: severe frost occurring with a large accumulated sum of effective temperatures resulted in full cone loss, and light frost substantially reduced cone number. A less important but significant climatic factor was September temperature: as the temperature increased, the cone number decreased in the following year. Over the last 30 years, the sum of the effective temperatures at which the last spring frost occurs, as well as the average September temperature, increased considerably, resulting in reduced cone production.

Conclusion – If the current climatic trend is maintained, and especially if it is strengthened, Siberian stone pine cone production in the southern boreal forest zone on the Western Siberian Plane is unlikely to provide for the effective renewal of the species.

Keywords
climate change, cone production dynamics, Siberian stone pine, spring frost, weather conditions

References

  • Barringer L.E., Tomback D.F., Wunder M.B. & McKinney S.T. 2012. Whitebark pine stand condition, tree abundance, and cone production as predictors of visitation by Clark’s nutcracker. PLoS ONE 7(5): e37663. https://doi.org/10.1371/journal.pone.0037663
  • Bisi F., Von Hardenberg J., Bertolino S., et al. 2016. Current and future conifer seed production in the Alps: testing weather factors as cues behind masting. European Journal of Forest Research 135: 743–754. https://doi.org/10.1007/s10342-016-0969-4
  • Bogdziewicz M., Kelli D., Thomas P.A., Lageard J.G.A. & Hacket-Pain A. 2020. Climate warming disrupts mast seeding and its fitness benefits in European beech. Nature Plants 6(2): 88–94. https://doi.org/10.1038/s41477-020-0592-8
  • Buechling A., Martin P.H., Canham C.D., Shepperd W.D. & Battaglia M.A. 2016. Climate drivers of seed production in Picea engelmannii and response to warming temperatures in the southern Rocky Mountains. Journal of Ecology 104(4): 1051–1062. https://doi.org/10.1111/1365-2745.12572
  • Carevic F.S., Fernández M., Alejano R., Vázquez-Piqué J., Tapias R. & Corral E. 2010. Plant water relations and edaphoclimatic conditions affecting acorn production in a holm oak (Quercus ilex L. ssp. ballota) open woodland. Agroforestry Systems 78: 299–308. https://doi.org/10.1007/s10457-009-9245-7
  • Crawley M.J. & Long C.R. 1995. Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. Journal of Ecology 83(4): 683–696.
  • Crone E.E. & Rapp J.M. 2014. Resource depletion, pollen coupling, and the ecology of mast seeding. Annals of the New York Academy of Sciences 1322: 21–34. https://doi.org/10.1111/nyas.12465
  • Delpierre N., Vitasse Y., Chuine I., et al. 2016. Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models. Annals of Forest Science 73: 5–25. https://doi.org/10.1007/s13595-015-0477-6
  • Fernández-Martínez M., Vicca S., Janssens I.A., Espelta J.M. & Peñuelas J. 2017. The North Atlantic Oscilation synchronises fruit production in Europian forests. Ecography 40(7): 864–874. https://doi.org/10.1111/ecog.02296
  • Goroshkevich S.N. 2008. Dynamics of growth and seed production in the Siberian stone pine: the level and pattern of variation in characters. Russian Journal of Ecology 39(2): 170–177. https://doi.org/10.1134/S1067413608020033
  • Goroshkevich S.N. 2017. Dynamics of Siberian stone pine (Pinus sibirica Du Tour) growth and seed production: cyclicity or acyclic oscillation? Tomsk State University Journal of Biology 38: 104–120. [In Russian, English summary]. https://doi.org/10.17223/19988591/38/6
  • Hallgren S.W. & Helms J.A. 1988. Control of height growth components in seedlings of California red and white fir by seed source and water stress. Canadian Journal of Forest Research 18(5): 521–529. https://doi.org/10.1139/x88-076
  • Herrera C.M., Jordano P., Guitián J. & Traveset A. 1998. Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. The American Naturalist 152(4): 576–594. https://doi.org/10.1086/286191
  • Hoch G., Siegwolf R.T., Keel S.G., Körner C. & Han Q. 2013. Fruit production in three masting tree species does not rely on stored carbon reserves. Oecologia 171(3): 653–662. https://doi.org/10.1007/s00442-012-2579-2
  • Houle G. 1999. Mast seeding in Abies balsamea, Acer saccharum and Betula alleghaniensis in an old growth, cold temperate forest of north-eastern North America. Journal of Ecology 87: 413–422. https://doi.org/10.1046/j.1365-2745.1999.00352.x
  • Iroshnikov A.I. 1974. Polymorphism of Siberian stone pine populations. In: Minina E.G. & Iroshnikov A.I. (eds) Variability of woody plants in Siberia: 77–103. Institute of Forestry and Timber SB USSR Academy of Sciences, Krasnoyarsk. [In Russian].
  • Juday G.P., Barber V., Rupp S., Zasada J.C. & Wilmking M. 2003. A 200-year perspective of climate variability and the response of white spruce in interior Alaska. In: Greenland D., Goodin D.G. & Smith R.C. (eds) Climate variability and ecosystem response at long-term ecological research sites: 226–250. Oxford University Press, Oxford.
  • Kaya Z., Adams W.T. & Campbell R.K. 1994. Adaptive significance of the intermittent pattern of shoot growth in Douglas-fir seedlings from southwest Oregon. Tree Physiology 14(11): 1277–1289. https://doi.org/10.1093/treephys/14.11.1277
  • Koenig W.D. & Knops J. 2005. The mystery of masting in trees: some trees reproduce synchronously over large areas, with widespread ecological effects, but how and why? American Scientist 93(4): 340–347. https://www.jstor.org/stable/27858609
  • Krebs C.J., Boonstra R., Cowcill K. & Kenney A.J. 2009. Climatic determinants of berry crops in the boreal forest of the southwestern Yukon. Botany 87(4): 401–408. https://doi.org/10.1139/B09-013
  • Krebs C.J., Cowcill K., Boonstra R. & Kenney A.J. 2010. Do changes in berry crops drive population fluctuations of rodentsin the southwestern Yukon? Journal of Mammalogy 91(2): 500–509. https://doi.org/10.1644/09-MAMM-A-005.1
  • Lanner R.M. 1982. Adaptations of whitebark pine for seed dispersal by Clark’s nutcracker. Canadian Journal of Forest Research 12(2): 391–402.
  • Lindner M., Maroschek M., Netherer S., et al. 2010. Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Forest Ecology and Management 259(4): 698–709. https://doi.org/10.1016/j.foreco.2009.09.023
  • Marino G.P., Kaiser D.P., Gu L. & Ricciuto D.M. 2011. Reconstruction of false spring occurrences over the southeastern United States, 1901–2007: an increasing risk of spring freeze damage? Environmental Research Letters 6(2): 024015. https://doi.org/10.1088/1748-9326/6/2/024015
  • Mishukov N.P. 1972. Cone production of Siberian stone pine in the northern taiga. Proceedings of the SB RAS. Series of Biological Sciences 15(3): 53–59. [In Russian].
  • Nekrasova T.P. 1972. Biological basis of the seed production in Siberian stone pine. Nauka, Novosibirsk. [In Russian].
  • Nekrasova T.P. 1983. Pollen and pollen order of conifers in Siberia. Nauka, Novosibirsk. [In Russian].
  • Nesvetajlo V.D. 1987. Long-term dynamics of reproductive activity and radial growth of Siberian stone pine in the stand from the southern taiga. Russian Journal of Ecology 6: 19–25. [In Russian].
  • Nussbaumer A., Waldner P., Apuhtin V., et al. 2018. Impact of weather cues and resource dynamics on mast occurrence in the main forest tree species in Europe. Forest Ecology and Management 429: 336–350. https://doi.org/10.1016/j.foreco.2018.07.011
  • Owens J.N. 2006. The reproductive biology of lodgepole pine. Forest Genetics Council of British Columbia, Extension Note 07.
  • Owens J.N. 2008. The reproductive biology of Western Larch. Forest Genetics Council of British Columbia, Extension Note 08.
  • Owens J.N. & Blake M.D. 1985. Forest tree seed production: a review of literature and recommendations for future research. Canadian Forestry Service Information Report PI-X-53: 161.
  • Owens J.N., Kittirat T. & Mahalovich M.F. 2008. Whitebark pine (Pinus albicaulis Engelm.) seed production in natural stands. Forest Ecology and Management 255(3–4): 803–809. https://doi.org/10.1016/j.foreco.2007.09.067
  • Pallardy S.G. 2007. Physiology of woody plants. Third edition. Academic Press, San Diego.
  • Pearse I.S., Koenig W.D. & Kelly D. 2016. Mechanisms of mast seeding: resources, weather, cues, and selection. New Phytologist 212(3): 546–562. https://doi.org/10.1111/nph.14114
  • Pearse I.S., LaMontagne J.M. & Koenig W.D. 2017. Inter-annual variation in seed production has increased over time (1900–2014). Proceedings of the Royal Society B 284(1868): 20171666. https://doi.org/10.1098/rspb.2017.1666
  • Pérez-Ramos I.M., Aponte C., García L.V., Padilla-Díaz C.M. & Marañón T. 2014. Why is seed production so variable among individuals? A ten-year study with oaks reveals the importance of soil environment. PLoS ONE 9(12): e115371. https://doi.org/10.1371/journal.pone.0115371
  • Pons J. & Pausas J.G. 2012. The coexistence of acorns with different maturation patterns explains acorn production variability in cork oak. Oecologia 169(3): 723–731. https://doi.org/10.1007/s00442-011-2244-1
  • Primack R.B. 1998. Essentials of conversation biology. Second edition. Sinauer Associates, Sunderland, Massachusetts.
  • Redmond M.D., Weisberg P.J., Cobb N.S., Gehring C.A., Whipple A.V. & Whitham T.G. 2016. A robust method to determine historical annual cone production among slow-growing conifers. Forest Ecology and Management 368: 1–6. https://doi.org/10.1016/j.foreco.2016.02.028
  • Richardson S.J., Allen R.B., Whitehead D., Carswell F.E., Ruscoe W.A. & Platt K.H. 2005. Climate and net carbon availability determine temporal patterns of seed production by Nothofagus. Ecology 86(4): 972–981. https://doi.org/10.1890/04-0863
  • Rohde A., Bastien C. & Boerjan W. 2011. Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiology 31(5): 472–482. https://doi.org/10.1093/treephys/tpr038
  • Roland C.A., Schmidt J.H. & Johnstone J.F. 2014. Climate sensitivity of reproduction in a mast-seeding boreal conifer across its distribution al range from lowland to treeline forests. Oecologia 174(3): 665–677. https://doi.org/10.1007/s00442-013-2821-6
  • Sakai A. & Malla S.B. 1981. Winter hardiness of tree species at high altitudes in the East Himalaya, Nepal. Ecology 62(5): 1288–1298. https://doi.org/10.2307/1937293
  • Schauber E.M., Kelly D., Turchin P., et al. 2002. Masting by eighteen New Zealand plant species: the role of temperature as a synchronizing cue. Ecology 83(5): 1214–1225. https://doi.org/10.2307/3071937
  • Sork V.L., Bramble J. & Sexton O. 1993. Ecology of mast-fruiting in three species of north American deciduous oaks. Ecology 74(2): 528–541. https://doi.org/10.2307/1939313
  • Speer J.H. 2010. Fundamentals of tree-ring research. University of Arizona Press, Tucson.
  • Tanino K.K., Kalcsits L., Silim S., Kendall E. & Gray G.R. 2010. Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Molecular Biology 73(1–2): 49–65. https://doi.org/10.1007/s11103-010-9610-y
  • Tretyakova I.N. 1990. Embryology of conifers: physiological aspects. Nauka, Novosibirsk. [in Russian].
  • Tretiyakova I.N. & Lukina N.V. 2016. Acceleration of embryonic development of Pinus sibirica trees with a one-year reproductive cycle. Ontogenez 47(1): 49–56. [In Russian]. https://doi.org/10.7868/S0475145016010067
  • Visser M.D., Jongejans E., van Breugel M., et al. 2001. Strict mast fruiting for a tropical dipterocarp tree: a demographic cost-benefit analysis of delayed reproduction and seed predation. Journal of Ecology 99(4): 1033–1044. https://doi.org/10.1111/j.1365-2745.2011.01825.x
  • Vorobjev V.N. 1983. Biological basis of complex exploitation of Siberian stone pine forests. Nauka, Novosibirsk. [in Russian].
  • Vorobjev V.N., Vorobjev N.A. & Goroshkevich S.N. 1989. Growth and sex of Siberian stone pine. Nauka, Novosibirsk. [in Russian].
  • Vorobjev V.N., Goroshkevich S.N. & Savchuk D.A. 1994. New trend in dendrochronology: method of retrospective study of seminiference dynamics in Pinaceae. In: Proceedings –International workshop on subalpine stone pines and their environment: the status of our knowledge; 1992 September 5–11; St.Moritz, Switzerland: 201–204. U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Ogden.
  • Zamorano J.G., Hokkanen T. & Lehikoinen A. 2018. Climate-driven synchrony in seed production of masting deciduous and conifer tree species. Journal of Plant Ecology 11(2): 180–188. https://doi.org/10.1093/jpe/rtw117
  • Zwiers F.W., Alexander L.V., Hegerl G.C., et al. 2013. Climate extremes: challenges in estimating and understanding recent changes in the frequency and intensity of extreme climate and weather events. In: Asrar G.R. & Hurrell J.W. (eds) Climate science for serving society: 339–389. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6692-1_13