Abstract
Key message
Norway spruce needle trait variation in natural populations along elevational gradient (980–1860 m a.s.l.) was driven more by environmental than genetic factors. Humid habitats conditioned higher mean values of morpho-anatomical needle traits in relation to dry habitats.
Abstract
Geographical and climatic characteristics (elevation, mean annual temperature, summer heat: moisture index, evaporation, climatic moisture deficit, growing degree-days, heating degree-days, de Martonne’s aridity index) drive variations in the morphological and anatomical traits of the Norway spruce (Picea abies L. Karst) needle (needle length, needle thickness, needle width, epidermis thickness with cuticle, hypodermis height, central bundle diameter, resin duct diameter, and the number of resin ducts). We studied the pattern of variation in these needle characteristics in 15 Balkan Mountains (BM) and Dinaric Alps (DA) natural populations (altitudes ranging from 1100 to 1860 and from 980 to 1530 m a.s.l., respectively). The needle traits showed significant differentiation between mountain regions, between populations and within populations. The largest contribution of genetic component in phenotypic variation had the needle length, both components had the same share in the needle width, whereas the environmental component of variability had the largest share in the other needle traits. The principal component analysis revealed that anatomical needle traits and the climatic conditions contributed to differences between populations from different mountain regions. An agglomerative hierarchical clustering analysis revealed three dendogram clusters: three BM populations made one cluster, DA populations made the second, whereas seven populations close to the BM populations and five close to the DA populations made the third cluster. Patterns of morpho-anatomical phenotypic variability point to selective mechanisms and adjustments, enable to define the boundaries of climate niches, and may provide a starting point for conservation program according to climate change projections in the Balkan region.
Similar content being viewed by others
References
Androsiuk P, Kaczmarek Z, Urbaniak L (2011) The morphological traits of needles as markers of geographical differentiation in European Pinus sylvestris populations. Dendrobiology 65:3–16
Bert D, Le Provost G, Delzon S, Plomion C, Gion JM (2021) Higher needle anatomic plasticity is related to better water-use efficiency and higher resistance to embolism in fast-growing Pinus pinaster families under water scarcity. Trees 35(1):287–306. https://doi.org/10.1007/s00468-020-02034-2
Caccianiga M, Compostella C (2012) Growth forms and age estimation of treeline species. Trees 26(2):331–342. https://doi.org/10.1007/s00468-011-0595-1
Colombo SJ (1998) Climatic warming and its effect on bud burst and risk of frost damage to white spruce in Canada. For Chron 74(4):567–577. https://doi.org/10.5558/tfc74567-4
De La Torre AR, Puiu D, Crepeau MW, Stevens K, Salzberg SL, Langley CH, Neale DB (2019a) Genomic architecture of complex traits in loblolly pine. New Phytol 221(4):1789–1801. https://doi.org/10.1111/nph.15535
De La Torre AR, Wilhite B, Neale DB (2019b) Environmental genome-wide association reveals climate adaptation is shaped by subtle to moderate allele frequency shifts in loblolly pine. Genome Biol Evol 11(10):2976–2989. https://doi.org/10.1093/gbe/evz220
De La Torre AR, Wilhite B, Puiu D, St Clair JB, Crepeau MW, Salzberg SL, Neale DB (2021) Dissecting the polygenic basis of cold adaptation using genome-wide association of traits and environmental data in Douglas-fir. Genes 12(1):110. https://doi.org/10.3390/genes12010110
de Tomás MS, Novák M, Klančnik K, Gaberšček A (2016) Spectral signatures of conifer needles mainly depend on their physical traits. Pol J Ecol 64:1–13. https://doi.org/10.3161/15052249PJE2016.64.1.001
England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broad-leaved evergreen species, Eucalyptus regnans. F Muell Trees 20:79–90. https://doi.org/10.1007/s00468-005-0015-5
Esteban LG, Martín JA, de Palacios P, Fernández FG, López R (2010) Adaptive anatomy of Pinus halepensis trees from different Mediterranean environments in Spain. Trees 24(1):19–30. https://doi.org/10.1007/s00468-009-0375-3
Falk W, Hempelmann N (2013) Species favourability shift in Europe due to climate change: a case study for Fagus sylvatica L. and Picea abies (L.) Karst. based on an ensemble of climate models. J Climatol 2013:1–18
Fernandez GCJ (1992) Residual analysis and data transformations: important tools in statistical analysis. Hortic Sci 27:297–300
Gachev E, Mitkov I (2017) Karstification in the mountains Durmitor (Montenegro) and Pirin (Bulgaria) and its expression in surface landforms. https://doi.org/10.15551/prgs.2017.50
Gebauer R, Volařík D, Urban J, Børja I, Nagy NE, Eldhuset TD, Krokene P (2011) Effect of thinning on anatomical adaptations of Norway spruce needles. Tree Physiol 31(10):1103–1113. https://doi.org/10.1093/treephys/tpr081
Goczał J, Oleksa A, Rossa R, Chybicki I, Meyza K, Plewa R, Tofilski A (2020) Climatic oscillations in quaternary have shaped the co-evolutionary patterns between the Norway spruce and its host-associated herbivore. Sci Rep 10(1):1–14. https://doi.org/10.1038/s41598-020-73272-0
Gömöry D, Zhelev P, Brus R (2020) The Balkans: a genetic hotspot but not a universal colonization source for trees. Plant Syst Evol 306(1):1–9. https://doi.org/10.1007/s00606-020-01647-x
Grulke NE (2010) Plasticity in physiological traits in conifers: implications for response to climate change in the western US. Environ Pollut 158(6):2032–2042. https://doi.org/10.1016/j.envpol.2009.12.010
Hamann A, Wang TL, Spittlehouse D, Murdock TQ (2013) A comprehensive, high-resolution database of historical and projected climate surfaces for Western North America. Bull Am Meteorol Soc 94:1307–1309. https://doi.org/10.1175/BAMS-D-12-00145.1
Huang Y, Mao J, Chen Z, Meng J, Xu Y, Duan A, Li Y (2016) Genetic structure of needle morphological and anatomical traits of Pinus yunnanensis. J for Res 27(1):13–25. https://doi.org/10.1007/s11676-015-0133-x
Jankowski A, Wyka TP, Żytkowiak R, Nihlgård B, Reich PB, Oleksyn J (2017) Cold adaptation drives variability in needle structure and anatomy in Pinus sylvestris L. along a 1,900 km temperate–boreal transect. Funct Ecol 31(12):2212–2223. https://doi.org/10.5061/dryad.001g4
Kašpar J, Hošek J, Treml V (2017) How wind affects growth in treeline Picea abies. Alp Bot 127(2):109–120. https://doi.org/10.1007/s00035-017-0186-x
Klančnik K, Vogel-Mikuš K, Gaberščik A (2014) Silicified structures affect leaf optical properties in grasses and sedge. J Photochem Photobiol B 130:1–10. https://doi.org/10.1016/j.jphotobiol.2013.10.011
Köbölkuti ZA, Tóth EG, Ladányi M, Höhn M (2017) Morphological and anatomical differentiation in peripheral Pinus sylvestris L. populations from the Carpathian region. Dendrobiology 77:105–117. https://doi.org/10.12657/denbio.077.009
Le Provost G, Domergue F, Lalanne C, Ramos Campos P, Grosbois A, Bert D, Meredieu C, Danjon F, Plomion C, Gion JM (2013) Soil water stress affects both cuticular wax content and cuticle-related gene expression in young saplings of maritime pine (Pinus pinaster Ait). BMC Plant Biol 13:95. https://doi.org/10.1186/1471-2229-13-95
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952. https://doi.org/10.1111/j.1365-2745.2006.01150.x
Lhotáková Z, Kopačková-Strnadová V, Oulehle F, Homolová L, Neuwirthová E, Švik M, Janoutová R, Albrechtová J (2021) Foliage biophysical trait predictionfrom laboratory spectra in Norway spruce is more affected by needle age than by site soil conditions. Remote Sens 13:3911–3924. https://doi.org/10.3390/rs13030391
Liu Y, El-Kassaby YA (2018) Evapotranspiration and favorable growing degree-days are key to tree height growth and ecosystem functioning: Meta-analyses of Pacific Northwest historical data. Sci Rep 8(1):1–12. https://doi.org/10.1038/s41598-018-26681-1
Lj M (2008) Šumarska entomologija. Univerzitet u Beogradu, Šumarski fakultet
Lukeš P, Stenberg P, Rautiainen M, Mottus M, Vanhatalo KM (2013) Optical properties of leaves and needles for boreal tree species in Europe. Remote Sens Lett 4:667–676. https://doi.org/10.1080/2150704X.2013.782112
Marquis B, Bergeron Y, Simard M, Tremblay F (2020) Probability of spring frosts, not growing degree-days, drives onset of spruce bud burst in plantations at the boreal-temperate forest ecotone. Front Plant Sci 11:1031. https://doi.org/10.3389/fpls.2020.01031
Miljković D, Stefanović M, Orlović S, Neđić MS, Kesić L, Stojnić S (2019) Wild cherry (Prunus avium (L.) L.) leaf shape and size variations in natural populations at different elevations. Alp Bot 129(2):163–174. https://doi.org/10.1007/s00035-019-00227-1
Naudiyal N, Wang J, Ning W, Gaire NP, Peili S, Yanqiang W, Ning S (2021) Potential distribution of Abies, Picea, and Juniperus species in the sub-alpine forest of Minjiang headwater region under current and future climate scenarios and its implications on ecosystem services supply. Ecol Indic 121:07–131. https://doi.org/10.1016/j.ecolind.2020.107131
Niinemets Ü, Keenan TF, Hallik L (2015) A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol 205(3):973–993. https://doi.org/10.1111/nph.13096
Nikolić B, Bojović S, Marin PD (2015) Variability of morpho-anatomical characteristics of the needles of Picea omorika from natural populations in Serbia. Plant Biosyst 149(1–2):61–67. https://doi.org/10.1080/11263504.2013.810180
Nikolić B, Bojović S, Marin PD (2016) Morpho-anatomical properties of Pinus heldreichii needles from natural populations in Montenegro and Serbia. Plant Biosyst 150(2):254–263. https://doi.org/10.1080/11263504.2014.984008
Nilsson O, Hjelm K, Nilsson U (2019) Early growth of planted Norway spruce and Scots pine after site preparation in Sweden. Scand J for Res 34(8):678–688. https://doi.org/10.1080/02827581.2019.1659398
Olascoaga B, Juurola E, Pinho P, Lukeš P, Halonen L, Nikinmaa E, Bäck J, Porcar-Castell A (2014) Seasonal variation in the reflectance of photosynthetically active radiation from epicuticular waxes of Scots pine (Pinus sylvestris) needles. Boreal Environ Res 19B:132
Pandey S (2021) Climatic influence on tree wood anatomy: a review. J Wood Sci 67(1):1–7. https://doi.org/10.1186/s10086-021-01956-w
Pensa M, Aalto T, Jalkanen R (2004) Variation in needle-trace diameter in respect of needle morphology in five conifer species. Trees Struct Funct 18:307–311. https://doi.org/10.1007/s00468-003-0307-6
Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855. https://doi.org/10.1111/j.1523-1739.1998.96489.x
Popović V, Lučić A, Rakonjac LJ, Maksimović Z, Ristić D (2020) Variability of morphological and anatomical characteristics of Serbian spruce (Picea omorika/Panč./Purkyne) needles of natural population located in the Milieševka river canyon. Genetika 52(3):1235–1248. https://doi.org/10.2298/GENSR2003235P
Poulos HM, Berlyn GP (2007) Variability in needle morphology and water status of Pinus cembroides across an elevational gradient in the Davis Mountains of west Texas, USA1. J Torrey Bot Soc 134(2):281–288. https://doi.org/10.3159/1095-5674(2007)134[281:VINMAW]2.0.CO
Radovanović B, Šinžar-Sekulić J, Rakić T, Živković I, Lakušić D (2014) Variation in needle anatomy of Picea omorika (Pinaceae) plants belonging to different gene pools in natural populations on Tara Mt. Serbia. Bot Serbica 38:237–246
Ravazzi C (2002) Late quaternary history of spruce in southern Europe. Rev Palaeobot Palynol 120(1–2):131–177. https://doi.org/10.1016/S0034-6667(01)00149-X
Rehfeldt GE, Ying CC, Spittlehouse DL, Hamilton DA Jr (1999) Genetic responses to climate in Pinus contorta: niche breadth, climate change, and reforestation. Ecol Monogr 69(3):375–407. https://doi.org/10.1890/0012-9615(1999)069[0375:GRTCIP]2.0.CO;2
Reich PB, Rich RL, Lu X, Wang YP, Oleksyn J (2014) Biogeographic variation in evergreen conifer needle longevity and impacts on boreal forest carbon cycle projections. Proc Nati Acad Sci USA 111(38):13703–13708. https://doi.org/10.1073/pnas.1216054110
Ruiz-Peinado R, Pretzsch H, Löf M, Heym M, Bielak K, Aldea J, del Río M (2021) Mixing effects on Scots pine (Pinus sylvestris L) and Norway spruce (Picea abies (L.) Karst.) productivity along a climatic gradient across Europe. For Ecol Manag 482:118834. https://doi.org/10.1016/j.foreco.2020.118834
Sáenz-Romero C, Kremer A, Nagy L, Újvári-Jármay É, Ducousso A, Kóczán-Horváth A, Hansen JK, Mátyás C (2019) Common garden comparisons confirm inherited differences in sensitivity to climate change between forest tree species. PeerJ 7:e6213. https://doi.org/10.7717/peerj.6213
SAS Institute, Inc. (2011) The SAS system for windows, release 9.3. SAS Institute, Cary
Schoettle AW, Rochelle SG (2000) Morphological variation of Pinus flexilis (Pinaceae), a bird-dispersed pine, across a range of elevations. Am J Bot 87(12):1797–1806. https://doi.org/10.2307/2656832
Sellin A (2000) Estimating the needle area from geometric measurements: application of different calculation methods to Norway spruce. Trees 14(4):215–222. https://doi.org/10.1007/PL00009765
Sheue CR, Yang YP, Huang Kuo- LL (2003) Altitudinal variation of resin ducts in Pinus taiwanensis Hayata (Pinaceae) needles. Bot Bull Acad Sin 44:305–313
Stanivuković Z, Vasiljević R (2018) Gradation of spruce bark beetles in the area of Han Pijesak. Bull Fac for Univ Banja Luka 28:29–36. https://doi.org/10.7251/GSF1828029S
Stojnić S, Avramidou EV, Fussi B, Westergren M, Orlović S, Matović B, Konnert M (2019) Assessment of genetic diversity and population genetic structure of Norway spruce (Picea abies (L.) Karsten) at its southern lineage in Europe. Implications for conservation of forest genetic resources. Forests 10(3):258. https://doi.org/10.3390/f10030258
Svystun T, Lundströmer J, Berlin M, Westin J, Jönsson AM (2021) Model analysis of temperature impact on the Norway spruce provenance specific bud burst and associated risk of frost damage. For Ecol Manag 493:119252. https://doi.org/10.1016/j.foreco.2021.119252
Thompson I, Mackey B, McNulty S, Mosseler A (2009) Forest resilience, biodiversity, and climate change. A synthesis of the biodiversity/resilience/stability in forest ecosystems. Secretariat of the convention on biological diversity, Montreal. Technical Deries 43, p 67
Tollefsrud MM, Kisslin R, Gugerli F, Johnsen Ø, Skrøppa T, Cheddadi R, van der Knaap WO, Latałowa M, TerHürne-Berson R, Litt T (2008) Genetic consequences of glacial survival and postglacial colonization in norway spruce: combined analysis of mitochondrial DNA and fossil pollen. Mol Ecol 17:4134–4150. https://doi.org/10.1111/j.1365-294X.2008.03893.x
Treml V, Kašpar J, Kuželová H, Gryc V (2015) Differences in intra-annual wood formation in Picea abies across the treeline ecotone, Giant Mountains, Czech Republic. Trees 29(2):515–526. https://doi.org/10.1007/s00468-014-1129-4
Urbaniak L, Karliński L, Popielarz R (2003) Variation of morphological needle characters of Scots pine (Pinus sylvestris L.) populations in different habitats. Acta Soc Bot Pol 72:37–44 (bwmeta1.element.agro-article-657f8dab-6839-4c59-9e71-7c65f6ee8f12)
Wahid N, González-Martínez SC, El Hadrami I, Boulli A (2006) Variation of morphological traits in natural populations of maritime pine (Pinus pinaster Ait.) in Morocco. Ann for Sci 63(1):83–92. https://doi.org/10.1051/forest:20050100
Wang T, Hamann A, Spittlehouse DL, Murdock TQ (2012) ClimateWNA—high-resolution spatial climate data for western North America. J Appl Meteorol Climatol 51(1):16–29. https://doi.org/10.1175/JAMC-D-11-043.1
Wang J, Ma J, OuYang F, Wang J, Song L, Kong L, Zhang H (2020) Instrinsic relationship among needle morphology, anatomy, gas exchanges and tree growth across 17 Picea species. New for. https://doi.org/10.1007/s11056-020-09808-z
Westergren M, Bozić G, Kraigher H (2018) Genetic diversity of core vs. peripheral Norway spruce native populations at a local scale in Slovenia. Iforest 11:104–110. https://doi.org/10.3832/ifor2444-011
Xing F, Mao JF, Meng J, Dai J, Zhao W, Liu H, Li Y (2014) Needle morphological evidence of the homoploid hybrid origin of Pinus densata based on analysis of artificial hybrids and the putative parents, Pinus tabuliformis and Pinus yunnanensis. Ecol Evol 4(10):1890–1902. https://doi.org/10.1002/ece3.1062
Zhang YX, Equiza MA, Zheng QS, Tyree MT (2012) Factors controlling plasticity of leaf morphology in Robinia pseudoacacia L. II: the impact of water stress on leaf morphology of seedlings grown in a controlled environment chamber. Ann for Sci 69:39–47. https://doi.org/10.1007/s13595-011-0134-7
Zhang M, Meng JX, Zhang ZJ, Zhu SL, Li Y (2017) Genetic analysis of needle morphological and anatomical traits among nature populations of Pinus tabuliformis. J Plant Stud. https://doi.org/10.5539/jps.v6n1p62
Acknowledgements
This study was supported by Ministry of Education, Science and Technological Development of Serbia, Contract numbers 451-03-9/2021-14/200027 and 451-03-9/2021-14/ 200007.
Author information
Authors and Affiliations
Contributions
The first author VP and last DM conceived the idea and designed the study, VP conducted fieldwork. BN anatomical sample preparation. LA and LJR project management responsibility for research. DŠJ substantial correction of the final manuscript version. DM writing the manuscript, performed statistical analyses, data curation, visualization results.
Corresponding author
Ethics declarations
Conflict of interest
The authors confirm that there is no conflict of interest in relation to this article.
Additional information
Communicated by Veronica De Micco .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Popović, V., Nikolić, B., Lučić, A. et al. Morpho-anatomical trait variability of the Norway spruce (Picea abies (L.) Karst.) needles in natural populations along elevational diversity gradient. Trees 36, 1131–1147 (2022). https://doi.org/10.1007/s00468-022-02277-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-022-02277-1