iForest - Biogeosciences and Forestry


Seed germination traits of Pinus heldreichii in two Greek populations and implications for conservation

Evangelia N Daskalakou (1)   , Katerina Koutsovoulou (2-3), Spyridon Oikonomidis (1-2), Costas A Thanos (2)

iForest - Biogeosciences and Forestry, Volume 15, Issue 4, Pages 331-338 (2022)
doi: https://doi.org/10.3832/ifor4045-015
Published: Aug 24, 2022 - Copyright © 2022 SISEF

Research Articles

Seed germination traits were assessed on Pinus heldreichii H. Christ, a Tertiary relict, high-elevation Mediterranean pine, endemic in the western Balkan Peninsula and southern Italy; it is naturally grown at the northern Greece mountains, but also found in shrubby form above the timberline. Closed and mature cones were collected (October) for three consecutive years from Pindos Range and Mt. Olympus populations. Cone and seed morphological traits were recorded along with the seedling cotyledon number. Seed germination tests were performed under various ecologically meaningful temperatures and light regimes; climate change effects on seed germination and seedling development were assessed based on two climate scenarios. Final seed germination was moderate (~55%) on both, untreated seed lots at most favourable conditions (15 and 20 °C). Although cold stratification is not an absolute requirement, seed germination rate and final percentage are promoted by both a month of cold stratification (at least 30 or 45 days) and white light. The predicted climate change suggests that a prolonged drought period (>3 months) might turn out by the end of the century in the populations studied. Although the temperature increase might not have significant effects in the germination window of the species. The rainfall decrease will inevitably expose the young seedlings to the summer drought, thus increasing the potential mortality rate. Both ex situ (e.g., germplasm conservation) and in situ measures of conservation are recommended for the species survival in Greece, with a particular focus on the populations established at lower altitudes.


Climate Change, Cold Stratification, Cotyledon Number, Heldreich’s Pine, Light Response, Seed Ecophysiology, Seed Mass

Authors’ address

Evangelia N Daskalakou 0000-0002-5190-1023
Spyridon Oikonomidis 0000-0003-4779-6897
Institute of Mediterranean and Forest Ecosystems, Hellenic Agricultural Organization “DEMETER”, Terma Alkmanos str., 11528 Athens (Greece)
Katerina Koutsovoulou
Spyridon Oikonomidis 0000-0003-4779-6897
Costas A Thanos 0000-0001-8748-8093
Department of Botany, Faculty of Biology, National and Kapodistrian University of Athens, Panepistimiopolis, 15784 Athens (Greece)
Katerina Koutsovoulou
Green Fund, Ministry of Environment and Energy, Villa Kazouli, Kifisias 241, 14561 Kifisia (Greece)

Corresponding author

Evangelia N Daskalakou


Daskalakou EN, Koutsovoulou K, Oikonomidis S, Thanos CA (2022). Seed germination traits of Pinus heldreichii in two Greek populations and implications for conservation. iForest 15: 331-338. - doi: 10.3832/ifor4045-015

Academic Editor

Gianluca Piovesan

Paper history

Received: Dec 23, 2021
Accepted: Jun 20, 2022

First online: Aug 24, 2022
Publication Date: Aug 31, 2022
Publication Time: 2.17 months

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 18012
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 15925
Abstract Page Views: 1251
PDF Downloads: 660
Citation/Reference Downloads: 1
XML Downloads: 175

Web Metrics
Days since publication: 633
Overall contacts: 18012
Avg. contacts per week: 199.18

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

(No citations were found up to date. Please come back later)


Publication Metrics

by Dimensions ©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

Arianoutsou M, Leone V, Moya D, Lovreglio R, Delipetrou P, De las Heras J (2012)
Management of threatened, high conservation value, forest hotspots under changing fire regimes. In: “Post-Fire Management and Restoration of Southern European Forests” (Moreira F, Corona P, Arianoutsou M, De las Heras J eds). Springer, Dordrecht, Netherlands, pp. 257-291.
CrossRef | Gscholar
Baskin CC, Baskin JM (2014)
Seeds, ecology, biogeography, and evolution of dormancy and germination (2nd edn). Academic Press, Elsevier, pp. 1586.
CrossRef | Gscholar
Bonanomi G, Rita A, Allevato E, Cesarano G, Saulino L, Di Pasquale G, Allegrezza M, Pesaresi S, Borghetti M, Rossi S, Saracino A (2018)
Anthropogenic and environmental factors affect the tree line position of Fagus sylvatica along the Apennines (Italy). Journal of Biogeography 45: 2595-2608.
CrossRef | Gscholar
Borghetti M, Vendramin GG, Veneziano A, Giannini R (1986)
Influence of stratification on germination of Pinus leucodermis. Canadian Journal of Forest Research 16: 867-896.
CrossRef | Gscholar
Borghetti M, Vendramin GG, Giannini R, Schettino A (1989)
Effects of stratification, temperature and light on germination of Pinus leucodermis. Acta Oecologica - Oecologia Plantarum 10: 45-56.
Online | Gscholar
Bryn A, Potthoff K (2018)
Elevational treeline and forest line dynamics in Norwegian mountain areas - a review. Landscape Ecology 33: 1225-1245.
CrossRef | Gscholar
Bucci G, Vendramin GG, Lelli L, Vicario F (1997)
Assessing the genetic divergence of Pinus leucodermis Ant. endangered populations: use of molecular markers for conservation purposes. Theoretical and Applied Genetics 7: 1138-1146.
CrossRef | Gscholar
Caković D, Gargano D, Matevski V, Shuka L (2017)
Pinus heldreichii. The IUCN Red List of Threatened Species 2017: e.T42368A95725658.
CrossRef | Gscholar
Cheddadi R, Araújo MB, Maiorano L, Edwards M, Guisan A, Carré M, Chevalier M, Pearman PB (2016)
Temperature range shifts for three European tree species over the last 10.000 years. Frontiers in Plant Science 7: 693.
CrossRef | Gscholar
Christensen KI (1997)
Pinus L. In: “Flora Hellenica” Vol. I (Strid A, Tan K eds). Koeltz Scientific Books, Koenigstein, Germany, pp. 4-9.
Chritchfield WB, Little EL (1966)
Geographic distribution of pines of the World. Miscellaneous Publication no. 991, USDA Forest Service, Washington, DC, USA, pp. 97.
Dantas BF, Moura MSB, Pelacani CR, Angelotti F, Taura TA, Oliveira GM, Bispo JS, Matias JR, Silva FFS, Pritchard HW, Seal CE (2020)
Rainfall, not soil temperature, will limit the seed germination of dry forest species with climate change. Oecologia 192: 529-541.
CrossRef | Gscholar
Daskalakou EN, Thanos CA (2010)
Postfire seedling dynamics and performance in Pinus halepensis Mill. populations. Acta Oecologica 36: 446-453.
CrossRef | Gscholar
Daskalakou EN, Koutsovoulou K, Ioannidis K, Koulelis PP, Ganatsas P, Thanos CA (2019)
Masting and regeneration dynamics of Abies cephalonica, the Greek endemic silver fir. Seed Science Research 29: 227-237.
CrossRef | Gscholar
Deslauriers A, Rossi S, Anfodillo T, Saracino A (2008)
Cambial phenology, wood formation and temperature thresholds in two contrasting years at high altitude in southern Italy. Tree Physiology 28: 863-871.
CrossRef | Gscholar
Dimopoulos P, Raus T, Bergmeier E, Constantinidis T, Iatrou G, Kokkini S, Strid A, Tzanoudakis D (2013)
Vascular plants of Greece: an annotated checklist. Botanischer Garten und Botanisches Museum Berlin€Dahlem, Freie Universität Berlin - Hellenic Botanical Society, Athens. Englera 31, pp. 370.
Fady B, Aravanopoulos FA, Alizoti P, Mátyás C, Von Wühlisch G, Westergren M, Belletti P, Cvjetkovic B, Ducci F, Huber G, Kelleher CT, Khaldi A, Bou Dagher Kharrat M, Kraigher H, Kramer K, Mühlethaler U, Peric S, Perry A, Rousi M, Sbay Stojnic H S, Tijardovic M, Tsvetkov I, Varela MC, Vendramin GG, Zlatanov T (2016)
Evolution-based approach needed for the conservation and silviculture of peripheral forest tree populations. Forest Ecology and Management 375: 66-75.
CrossRef | Gscholar
Farjon A (2018)
Pines. Drawings and descriptions of the genus Pinus. Brill, Leiden, Boston, MA, USA, pp. 101.
CrossRef | Gscholar
Gehrig-Fasel J, Guisan A, Zimmermann NE (2007)
Tree line shifts in the Swiss Alps: climate change or land abandonment? Journal of Vegetation Science 18: 571-582.
CrossRef | Gscholar
Giannini R, Bellari C (1995)
Heritability estimate of seed germination parameters in Pinus leucodermis Antoine. Seed Science and Technology 23: 385-392.
Online | Gscholar
IPCC (2021)
Climate change 2021: the physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B eds). Cambridge University Press, Cambridge, UK.
ISTA (2007)
International rules for seed testing. International Seed Testing Association, Bassersdorf, Switzerland, pp. 5A-37.
Janssen JAM, Rodwell JS, Garcia Criado M, Gubbay S, Haynes T, Nieto A, Sanders N, Landucci F, Loidi J, Ssymank A, Tahvanainen T, Valderrabano M, Acosta A, Aronsson M, Arts G, Attorre F, Bergmeier E, Bijlsma R-J, Bioret F, Nicolae C, Biurrun I, Calix M, Capelo J, Chytry M, Dengler J, Dimopoulos P, Essl F, Gardfjell H, Gigante D, Giusso Del Galdo G, Hajek M, Jansen F, Jansen J, Kapfer J, Mickolajczak A, Molina JA, Molnar Z, Paternoster D, Piernik A, Poulin B, Renaux B, Schaminee J, Toivonen H, Tonteri T, Tsiripidis I, Tzonev R, Valachovič M (2016)
European red list of habitats - Part 2. Terrestrial and freshwater habitats. Publications Office of the European Union, Luxembourg, pp. 38.
Online | Gscholar
Jin WT, Gernandt DS, Wehenkel C, Xia XM, Wei XX, Wang XQ (2021)
Phylogenomic and ecological analyses reveal the spatiotemporal evolution of global pines. Proceedings of the National Academy of Sciences USA 118: 49 (e2022302118).
CrossRef | Gscholar
Klippel L, Krusic PJ, Brandes R, Hartl-Meier C, Trouet V, Meko M, Esper J (2017)
High-elevation inter-site differences in Mount Smolikas tree-ring width data. Dendrochronologia 44: 164-173.
CrossRef | Gscholar
Krugman SL, Jenkinson JL (2008)
Pinaceae-Pine family: Pinus L. In: “The Woody Plant Seed Manual” (Bonner FT, Karrfalt RP eds). Agriculture Handbook no. 727, USDA Forest Service, Washington, DC, USA, pp. 809-847.
Kullman L (2002)
Rapid recent range-margin rise of tree and shrub species in the Swedish Scandes. Journal of Ecology 90: 68-77.
CrossRef | Gscholar
Lett S, Dorrepaal E (2018)
Global drivers of tree seedling establishment at alpine treelines in a changing climate. Functional Ecology 32: 1666-1680.
CrossRef | Gscholar
Ne’eman G, Arianoutsou M (2021)
Mediterranean pines - Adaptations to fire. In: “Pines and their Mixed Forest Ecosystems in the Mediterranean Basin. Managing Forest Ecosystems” (Ne’eman G, Osem Y eds). Springer, Cham, Switzerland, pp. 457-480.
CrossRef | Gscholar
R Development Core Team (2005)
R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Online | Gscholar
Riahi K, Vuuren DPV, Kriegler E, Edmonds J, Neil BCO, Fujimori S, Bauer N, Calvin K, Dellink R, Fricko O, Lutz W, Popp A, Cuaresma JC, Samir KC, Leimbach M, Jiang L, Kram T, Rao S, Emmerling J, Ebi K, Hasegawa T, Havlik P, Humpenoder F, Silva LAD, Smith S, Stehfest E, Bosetti V, Eom J, Gernaat D, Masui T, Rogelj J, Strefler J, Drouet L, Krey V, Luderer G, Harmsen M, Takahashi K, Baumstark L, Doelman JC, Kainuma M, Klimont Z, Marangoni G, Campen HL, Obersteiner M, Tabeau A, Tavoni M (2017)
The shared socioeconomic pathways and their energy, land use, and greenhouse gas emissions implications: an overview. Global Environmental Change 42: 153-168.
CrossRef | Gscholar
Rivers MC, Beech E, Bazos I, Bogunić F, Buira A, Caković D, Carapeto A, Carta A, Cornier B, Fenu G, Fernandes F, Fraga P, Garcia Murillo PJ, Lepší M, Matevski V, Medina FM, Menezes De Sequeira M, Meyer N, Mikoláš V, Montagnani C, Monteiro-Henriques T, Naranjo Suárez J, Orsenigo S, Petrova A, Reyes-Betancort JA, Rich T, Salvesen PH, Santana López I, Scholz S, Sennikov A, Shuka L, Silva LF, Thomas P, Troia A, Villar JL, Allen DJ (2019)
European red list of trees. IUCN, Cambridge, UK and Brussels, Belgium, pp. 72.
Online | Gscholar
Saeed M (2000)
Comparative physiology and ecophysiology of regeneration (germination, reproduction, reproductive potential) of genus Pinus. PhD Thesis, Department of Botany, Faculty of Biology, University of Athens, Greece, pp. 211.
Savolainen O, Kujala ST, Sokol C, Pyhäjärvi T, Avia K, Knürr T, Kärkkäinen K, Hicks S (2011)
Adaptive potential of northernmost tree populations to climate change, with emphasis on Scots pine (Pinus sylvestris L.). Journal of Heredity 102: 526-536.
CrossRef | Gscholar
Séférian R, Nabat P, Michou M, Martin DS, Voldoire A, Colin J, Decharme B, Delire C, Berthet S, Chevallier M, Sénési S, Franchisteguy L, Vial J, Mallet M, Joetzjer E, Geoffroy O, Guérémy JF, Moine MP, Msadek R, Ribes A, Rocher M, Roechrig R, Salas-y-Mélia D, Sanchez E, Terray L, Vaclke S, Waldman R, Aumont O, Bopp L, Deshayes J, Ethé C, Madec G (2019)
Evaluation of CNRM earth system model, CNRM-ESM2-1: role of earth system processes in present-day and future climate. Journal of Advances in Modelling Earth Systems 11: 4182-4227.
CrossRef | Gscholar
Skordilis A, Thanos CA (1997)
Comparative ecophysiology of seed germination strategies in the seven pine species naturally growing in Greece. In: “Basic and Applied Aspects of Seed Biology” (Summerfield RJ, Ellis RH, Black M, Murdoch AJ, Hong TD eds). Current Plant Science and Biotechnology in Agriculture, vol. 30, Springer, Dordrecht, Netherlands, pp. 623-632.
CrossRef | Gscholar
Skourti E, Thanos CA (2015)
Seed after ripening and germination photoinhibition in the genus Crocus (Iridaceae). Seed Science Research 25: 306-320.
CrossRef | Gscholar
Stojicic D, Golubovic-Curguz V, Veselinovic M (2004)
Possibility of greybark pine (Pinus heldreichii Christ.) seedling production in nurseries. In: Proceedings of the International Conference “75 Years of the Forest Research Institute of the Bulgarian Academy of Sciences”. Sofia (Bulgaria) 1-5 Oct 2003, vol. 2, pp. 37-41.
Stojičić D, Janošević D, Uzelac B, Budimir S (2008)
Factors influencing germination and growth of isolated embryos of Pinus heldreichii. Archives of Biological Sciences 60: 673-679.
CrossRef | Gscholar
Thanos CA, Doussi MA (1995)
Ecophysiology of seed germination in endemic labiates of Crete. Israel Journal of Plant Sciences 43: 227-237.
CrossRef | Gscholar
Thanos CA (2000)
Ecophysiology of seed germination in Pinus halepensis and P. brutia. In: “Ecology, Biogeography and Management of Pinus halepensis and P. brutia Forest Ecosystems in the Mediterranean Basin” (Ne’eman G, Trabaud L eds). Backhuys Publishers, Leiden, Netherlands, pp. 37-50.
Thanos CA, Fournaraki C (2010)
Global warming and seed germination - the case of Nepeta sphaciotica, an alpine Cretan endemic. Seed Ecology III. In: Proceedings of the International Society for Seed Science Meeting “Seeds and Change” (Pendleton R, Meyer S, Schultz B eds). Salt Lake City (Utah, USA), 20-24 June 2010. USDA Forest Service, Rocky Mountain Research Station, Albuquerque, NM, USA, pp. 176-177.
Vendramin GG, Fineschi S, Fady B (2008)
EUFORGEN Technical Guidelines for genetic conservation and use for Heldreich’s pine (Pinus heldreichii). Biodiversity International, Rome, Italy, pp. 6.
Vidakovic M (1991)
Pinus heldreichii Christ. - Heldreich Pine. In: “Conifers: Morphology and Variation” (Boro Brekalo ed). Graficki Zadov-Hrvatske, Yugoslavia, pp. 450-458.
Vitali A, Garbarino M, Camarero JJ, Malandra F, Toromani E, Spalevic V, Urbinati C (2019)
Pine recolonization dynamics in Mediterranean human-disturbed treeline ecotones. Forest Ecology and Management 435: 28-37.
CrossRef | Gscholar
Walck JL, Hidayati SN, Dixon KW, Thompson K, Poschlod P (2011)
Climate change and plant regeneration from seed. Global Change Biology 17: 2145-2161.
CrossRef | Gscholar
Walter H, Lieth HHF (1967)
Klimadiagramm - weltatlas [World Climate Diagram]. VEB Gustav Fischer Verlag, Germany. [in German]
WorldClim (2020)
Global climate data, free climate data for ecological modeling and GIS (version 2.1). Web site.
Online | Gscholar
Xystrakis F, Theodoropoulos K, Eleftheriadou E, Reif A (2006)
The vegetation of forest and shrubland with creeping Pinus heldreichii in Elikodromio, Olympus National Park, Greece. In: Proceedings of the IV Balkan Botanical Congress “Plant, fungal and habitat diversity investigation and conservation” (Ivanova D ed), Sofia (Bulgaria) 20-26 June 2006, pp. 345-352.

This website uses cookies to ensure you get the best experience on our website. More info