Influence of Spatiotemporal Dynamics on the Fine-Scale Spatial Genetic Structure of Differently Managed Picea abies Stands
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Area
2.2. Sampling Strategy and Genotyping
2.3. Spatial Data Analysis
2.4. Genetic Data Analysis
2.5. Relationship between Age and Fine-Scale SGS
3. Results
3.1. Spatial Distribution of Individual Age
3.2. Spatial Distribution of Genetic Variation
3.3. Relationship between Age and Fine-Scale SGS
4. Discussion
4.1. Influence of Forest Management on the Spatial and Age Structure
4.2. Influence of Forest Management on the Fine-Scale Spatial Genetic Structure
4.3. Effect of Spatiotemporal Dynamics on the Fine-Scale Spatial Genetic Structure
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Franklin, J.F.; Lindenmayer, D.; Thornburgh, D.; van Pelt, R.; Chen, J.; Spies, T.A.; Carey, A.B.; Shaw, D.C.; Berg, D.R.; Harmon, M.E.; et al. Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. For. Ecol. Manag. 2002, 155, 399–423. [Google Scholar] [CrossRef]
- Motta, R.; Garbarino, M.; Berretti, R.; Meloni, F.; Nosenzo, A.; Vacchiano, G. Development of old-growth characteristics in uneven-aged forests of the Italian Alps. Eur. J. For. Res. 2015, 134, 19–31. [Google Scholar] [CrossRef]
- Moeur, M. Characterizing spatial patterns of trees using stem-mapped data. For. Sci. 1993, 39, 756–775. [Google Scholar]
- Adams, W.T.; Zuo, J.; Shimizu, J.Y.; Tappeiner, J.C. Impact of alternative regeneration methods on genetic diversity in coastal Douglas-fir. For. Sci. 1998, 44, 390–396. [Google Scholar]
- Rajora, O.P. Genetic biodiversity impacts of silvicultural practices and phenotypic selection in white spruce. Theor. Appl. Genet. 1999, 99, 954–961. [Google Scholar] [CrossRef]
- Epperson, B.K.; Chung, M.G. Spatial genetic structure of allozyme polymorphisms within populations of Pinus strobus (Pinaceae). Am. J. Bot. 2001, 88, 1006–1010. [Google Scholar] [CrossRef] [PubMed]
- Marquardt, P.E.; Epperson, B.K. Spatial and population genetic structure of microsatellites in white pine. Mol. Ecol. 2004, 13, 3305–3315. [Google Scholar] [CrossRef] [PubMed]
- Marquardt, P.E.; Echt, C.S.; Epperson, B.K.; Pubanz, D.M. Genetic structure, diversity, and inbreeding of eastern white pine under different management conditions. Can. J. For. Res. 2007, 37, 2652–2662. [Google Scholar] [CrossRef]
- Kavaliauskas, D.; Fussi, B.; Westergren, M.; Aravanopoulos, F.; Finzgar, D.; Baier, R.; Alizoti, P.; Bozic, G.; Avramidou, E.; Konnert, M.; et al. The interplay between forest management practices, genetic monitoring, and other long-term monitoring systems. Forests 2018, 9, 133. [Google Scholar] [CrossRef]
- Neale, D.B. Genetic implications of shelterwood regeneration of Douglas-fir in Southwest Oregon. For. Sci. 1985, 15, 995–1005. [Google Scholar]
- Piotti, A.; Leonardi, S.; Heuertz, M.; Buiteveld, J.; Geburek, T.; Gerber, S.; Kramer, K.; Vettori, C.; Vendramin, G.G. Within-population genetic structure in beech (Fagus sylvatica L.) stands characterized by different disturbance histories: Does forest management simplify population substructure? PLoS ONE 2013, 8, e73391. [Google Scholar] [CrossRef] [PubMed]
- Piotti, A. The genetic consequences of habitat fragmentation: The case of forests. iForest—Biogeosci. For. 2009, 2, 75–76. [Google Scholar] [CrossRef]
- Lowe, A.J.; Cavers, S.; Boshier, D.; Breed, M.F.; Hollingsworth, P.M. The resilience of forest fragmentation genetics—No longer a paradox—We were just looking in the wrong place. Heredity 2015, 115, 97–99. [Google Scholar] [CrossRef] [PubMed]
- Rajendra, K.C.; Seifert, S.; Prinz, K.; Gailing, O.; Finkeldey, R. Subtle human impacts on neutral genetic diversity and spatial patterns of genetic variation in European beech (Fagus sylvatica). For. Ecol. Manag. 2014, 319, 138–149. [Google Scholar] [CrossRef]
- Sjölund, M.J.; Jump, A.S. Coppice management of forests impacts spatial genetic structure but not genetic diversity in European beech (Fagus sylvatica L.). For. Ecol. Manag. 2015, 336, 65–71. [Google Scholar] [CrossRef]
- Lamedica, S.; Lingua, E.; Popa, I.; Motta, R.; Carrer, M. Spatial structure in four Norway spruce stands with different management history in the Alps and Carpathians. Silva Fenn. 2011, 45, 865–873. [Google Scholar] [CrossRef]
- Westergren, M.; Bozic, G.; Ferreira, A.; Kraigher, H. Insignificant effect of management using irregular shelterwood system on the genetic diversity of European beech (Fagus sylvatica L.): A case study of managed stand and old growth forest in Slovenia. For. Ecol. Manag. 2015, 335, 51–59. [Google Scholar] [CrossRef]
- Bontemps, A.; Klein, E.K.; Oddou-Muratorio, S. Shift of spatial patterns during early recruitment in Fagus sylvatica: Evidence from seed dispersal estimates based on genotypic data. For. Ecol. Manag. 2013, 305, 67–76. [Google Scholar] [CrossRef]
- Troupin, D.; Nathan, R.; Vendramin, G.G. Analysis of spatial genetic structure in an expanding Pinus halepensis population reveals development of fine-scale genetic clustering over time. Mol. Ecol. 2006, 15, 3617–3630. [Google Scholar] [CrossRef] [PubMed]
- Lesser, M.R.; Parchman, T.L.; Jackson, S.T. Development of genetic diversity, differentiation and structure over 500 years in four ponderosa pine populations. Mol. Ecol. 2013, 22, 2640–2652. [Google Scholar] [CrossRef] [PubMed]
- King, G.M.; Gugerli, F.; Fonti, P.; Frank, D.C. Tree growth response along an elevational gradient: Climate or genetics? Oecologia 2013, 173, 1587–1600. [Google Scholar] [CrossRef] [PubMed]
- Bosela, M.; Popa, I.; Gömöry, D.; Longauer, R.; Tobin, B.; Kyncl, J.; Kyncl, T.; Nechita, C.; Petráš, R.; Sidor, C.G.; et al. Effects of post-glacial phylogeny and genetic diversity on the growth variability and climate sensitivity of European silver fir. J. Ecol. 2016, 104, 716–724. [Google Scholar] [CrossRef]
- Heer, K.; Behringer, D.; Piermattei, A.; Bässler, C.; Brandl, R.; Fady, B.; Jehl, H.; Liepelt, S.; Lorch, S.; Piotti, A.; et al. Linking dendroecology and association genetics in natural populations: Stress responses archived in tree rings associate with SNP genotypes in silver fir (Abies alba Mill.). Mol. Ecol. 2018, 27, 1428–1438. [Google Scholar] [CrossRef] [PubMed]
- Avanzi, C.; Piermattei, A.; Piotti, A.; Büntgen, U.; Heer, K.; Opgenoorth, L.; Spanu, I.; Urbinati, C.; Vendramin, G.G.; Leonardi, S. Disentangling the effects of spatial proximity and genetic similarity on individual growth performances in Norway spruce natural populations. Sci. Total Environ. 2019, 650, 493–504. [Google Scholar] [CrossRef] [PubMed]
- Lorimer, C.G.; Frelich, L.E. A methodology for estimating canopy disturbance frequency and intensity in dense temperate forests. Can. J. For. Res. 1989, 19, 651–663. [Google Scholar] [CrossRef]
- Carrer, M.; Urbinati, C. Age-dependent tree-ring growth responses to climate in Larix decidua and Pinus cembra. Ecology 2004, 85, 730–740. [Google Scholar] [CrossRef]
- Primicia, I.; Camarero, J.J.; Janda, P.; Čada, V.; Morrissey, R.C.; Trotsiuk, V.; Bače, R.; Teodosiu, M.; Svoboda, M. Age, competition, disturbance and elevation effects on tree and stand growth response of primary Picea abies forest to climate. For. Ecol. Manag. 2015, 354, 77–86. [Google Scholar] [CrossRef]
- Rita, A.; Borghetti, M.; Todaro, L.; Saracino, A. Interpreting the Climatic Effects on Xylem Functional Traits in Two Mediterranean Oak Species: The Role of Extreme Climatic Events. Front. Plant Sci. 2016, 7, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Motta, R.; Nola, P.; Piussi, P. Structure and stand development in three subalpine Norway spruce (Picea abies (L.) Karst.) stands in Paneveggio (Trento, Italy). Glob. Ecol. Biogeogr. 1999, 8, 455–471. [Google Scholar] [CrossRef]
- Duncker, P.S.; Barreiro, S.M.; Hengeveld, G.M.; Lind, T.; Mason, W.L.; Ambrozy, S. Classification of Forest Management Approaches: A New Conceptual Framework and Its Applicability to European Forestry. Ecol. Soc. 2012, 17, 51. [Google Scholar] [CrossRef]
- Altman, J.; Hédl, R.; Szabó, P.; Mazůrek, P.; Riedl, V.; Müllerová, J.; Kopecký, M.; Doležal, J. Tree-rings mirror management legacy: Dramatic response of standard oaks to past coppicing in Central Europe. PLoS ONE 2013, 8, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Austerlitz, F.; Mariette, S.; Machon, N.; Gouyon, P.H.; Godelle, B. Effects of colonization process on genetic diversity: Differences between annual plant and tree species. Genetics 2000, 154, 1309–1321. [Google Scholar] [PubMed]
- Motta, R. Old-growth forests and silviculture in the Italian Alps: The case-study of the strict reserve of Paneveggio (TN). Plant Biosyst. 2002, 136, 223–231. [Google Scholar] [CrossRef]
- Motta, R.; Nola, P.; Piussi, P. Long-term investigations in a strict forest reserve in the eastern Italian Alps: Spatio-temporal origin and development in two multi-layered subalpine stands. J. Ecol. 2002, 90, 495–507. [Google Scholar] [CrossRef]
- Di Tommaso, P.L. Contributo ad una tipologia floristicoecologica della foresta di Paneveggio (Trento). Versante meridionale. Ann. Accad. Ital. Sci. For. 1983, 32, 287–315. [Google Scholar]
- Motta, R.; Nola, P. Fraying damages in the subalpine forest of Paneveggio (Trento, Italy): A dendroecological approach. For. Ecol. Manag. 1996, 88, 81–86. [Google Scholar] [CrossRef]
- Scotti, I.; Paglia, G.P.; Magni, F.; Morgante, M. Efficient development of dinucleotide microsatellite markers in Norway spruce (Picea abies Karst.) through dot-blot selection. Theor. Appl. Genet. 2002, 104, 1035–1041. [Google Scholar] [CrossRef] [PubMed]
- Pfeiffer, A.; Olivieri, A.; Morgante, M. Identification and characterization of microsatellites in Norway spruce (Picea abies K.). Genome 1997, 40, 411–419. [Google Scholar] [CrossRef] [PubMed]
- Piotti, A.; Leonardi, S.; Piovani, P.; Scalfi, M.; Menozzi, P. Spruce colonization at treeline: Where do those seeds come from. Heredity 2009, 103, 136–145. [Google Scholar] [CrossRef] [PubMed]
- Shimatani, K. Point processes for fine-scale spatial genetics and molecular ecology. Biom. J. 2002, 44, 325–352. [Google Scholar] [CrossRef]
- Wiegand, T.; Moloney, K.A. Handbook of Spatial Point-pattern Analysis in Ecology; Chapman and Hall/CRC: New York, NY, USA, 2014. [Google Scholar]
- Stoyan, D.; Stoyan, H. Fractals, Random Shapes, and Point Fields: Methods of Geometrical Statistics; Wiley: Chichester, UK, 1994. [Google Scholar]
- Wiegand, T.; Moloney, K.A. Rings, circles, and null-models for point pattern analysis in ecology. Oikos 2004, 104, 209–229. [Google Scholar] [CrossRef] [Green Version]
- Diggle, P.J. Statistical Analysis of Spatial Point Patterns; Edward Arnold: London, UK, 2003. [Google Scholar]
- Getis, A.; Ord, J.K. The analysis of spatial association by use of distance statistics. Geogr. Anal. 1992, 24, 189–206. [Google Scholar] [CrossRef]
- Carrer, M.; Soraruf, L.; Lingua, E. Convergent space-time tree regeneration patterns along an elevation gradient at high altitude in the Alps. For. Ecol. Manag. 2013, 304, 1–9. [Google Scholar] [CrossRef]
- Sawada, M. Rookcase: An Excel 97/2000 Visual Basic (VB) add-in for exploring global and local spatial autocorrelation. Bull. Ecol. Soc. Am. 1999, 80, 231–234. [Google Scholar]
- Peakall, R.; Smouse, P.E. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics 2012, 28, 2537–2539. [Google Scholar] [CrossRef] [PubMed]
- Kalinowski, S.T. hp-rare 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 2005, 5, 187–189. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018. [Google Scholar]
- Loiselle, B.A.; Sork, V.L.; Nason, J.; Graham, C. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am. J. Bot. 1995, 82, 1420–1425. [Google Scholar] [CrossRef]
- Hardy, O.J.; Vekemans, X. SPAGeDi: A versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2002, 2, 618–620. [Google Scholar] [CrossRef]
- Vekemans, X.; Hardy, O.J. New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 2004, 13, 921–935. [Google Scholar] [CrossRef] [PubMed]
- Guillot, G.; Mortier, F.; Estoup, A. Geneland: A computer package for landscape genetics. Mol. Ecol. Notes 2005, 5, 712–715. [Google Scholar] [CrossRef]
- Guillot, G.; Santos, F.; Estoup, A. Analysing georeferenced population genetics data with Geneland: A new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 2008, 24, 1406–1407. [Google Scholar] [CrossRef] [PubMed]
- Schoenenberger, W.; Kuhn, N.; Laessig, R. Research Objectives and Projects on Windthrow Areas in Switzerland; AGRIS: Zurich, Switzerland, 1995. [Google Scholar]
- Motta, R.; Lingua, E. Human impact on size, age, and spatial structure in a mixed European larch and Swiss stone pine forest in the Western Italian Alps. Can. J. For. Res. 2005, 35, 1809–1820. [Google Scholar] [CrossRef]
- Resler, L.M.; Butler, D.R.; Malanson, G.P. Topographic shelter and conifer establishment and mortality in an alpine environment, Glacier National Park, Montana. Phys. Geogr. 2005, 26, 112–125. [Google Scholar] [CrossRef]
- Maher, E.L.; Germino, M.J. Microsite differentiation among conifer species during seedling establishment at alpine treeline. Ecoscience 2006, 13, 334–341. [Google Scholar] [CrossRef] [Green Version]
- Kuuluvainen, T. Gap disturbance, ground microtopography, and the regeneration dynamics of boreal coniferous forests in Finland: A review. Ann. Zool. Fenn. 1994, 31, 35–51. [Google Scholar]
- Holtmeier, F.K. Mountain Timberlines: Ecology, Patchiness, and Dynamics; Springer Science & Business Media: Berlin, Germany, 2009; Volume 36. [Google Scholar]
- Ratnam, W.; Rajora, O.P.; Finkeldey, R.; Aravanopoulos, F.; Bouvet, J.-M.; Vaillancourt, R.E.; Kanashiro, M.; Fady, B.; Tomita, M.; Vinson, C. Genetic effects of forest management practices: Global synthesis and perspectives. For. Ecol. Manag. 2014, 333, 52–65. [Google Scholar] [CrossRef]
- Aravanopoulos, F. Do silviculture and forest management affect the genetic diversity and structure of long-impacted forest tree populations? Forests 2018, 9, 355. [Google Scholar] [CrossRef]
- Motta, R.; Berretti, R.; Castagneri, D.; Lingua, E.; Nola, P.; Vacchiano, G. Stand and coarse woody debris dynamics in subalpine Norway spruce forests withdrawn from regular management. Ann. For. Sci. 2010, 67, 803. [Google Scholar] [CrossRef]
- Maghuly, F.; Pinsker, W.; Praznik, W.; Fluch, S. Genetic diversity in managed subpopulations of Norway spruce [Picea abies (L.) Karst.]. For. Ecol. Manag. 2006, 222, 266–271. [Google Scholar] [CrossRef]
- Unger, G.M.; Konrad, H.; Geburek, T. Does spatial genetic structure increase with altitude? An answer from Picea abies in Tyrol, Austria. Plant Syst. Evol. 2011, 292, 133–141. [Google Scholar] [CrossRef]
- Evans, M.E.K.; Gugger, P.F.; Lynch, A.M.; Guiterman, C.H.; Fowler, J.C.; Klesse, S.; Riordan, E.C. Dendroecology meets genomics in the common garden: New insights into climate adaptation. New Phytol. 2018, 218, 401–403. [Google Scholar] [CrossRef] [PubMed]
- Trujillo-Moya, C.; George, J.-P.; Fluch, S.; Geburek, T.; Grabner, M.; Karanitsch-Ackerl, S.; Konrad, H.; Mayer, K.; Sehr, E.M.; Wischnitzki, E.; et al. Drought sensitivity of Norway spruce at the species’ warmest fringe: Quantitative and molecular analysis reveals high genetic variation among and within provenances. G3: Genes Genomes Genet. 2018, 8, 1225–1245. [Google Scholar] [CrossRef] [PubMed]
- Housset, J.M.; Nadeau, S.; Isabel, N.; Depardieu, C.; Duchesne, I.; Lenz, P.; Girardin, M.P. Tree rings provide a new class of phenotypes for genetic associations that foster insights into adaptation of conifers to climate change. New Phytol. 2018, 218, 630–645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leonarduzzi, C.; Piotti, A.; Spanu, I.; Vendramin, G.G. Effective gene flow in a historically fragmented area at the southern edge of silver fir (Abies alba Mill.) distribution. Tree Genet. Genomes 2016, 12, 95. [Google Scholar] [CrossRef]
Plot | N Spatial Analysis 1 | N Genetic Analysis | Elevation (m a.s.l.) | Regeneration Density (n ha−1) | Past Management | Last Intervention | Na | HE | Ar100 |
---|---|---|---|---|---|---|---|---|---|
VB1 | 479 | 97 | 1695 | 935 | Wood production | 1984 | 10 | 0.64 | 8.87 |
VB2 | 541 | 114 | 1815 | 30 | Wood production | 1948 | 11.4 | 0.64 | 9.34 |
VB3 | 452 | 117 | 1865 | 3010 | Wood pasture | 1929 | 10.6 | 0.64 | 9.21 |
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Piotti, A.; Garbarino, M.; Avanzi, C.; Berretti, R.; Motta, R.; Piovani, P.; Leonardi, S. Influence of Spatiotemporal Dynamics on the Fine-Scale Spatial Genetic Structure of Differently Managed Picea abies Stands. Forests 2018, 9, 622. https://doi.org/10.3390/f9100622
Piotti A, Garbarino M, Avanzi C, Berretti R, Motta R, Piovani P, Leonardi S. Influence of Spatiotemporal Dynamics on the Fine-Scale Spatial Genetic Structure of Differently Managed Picea abies Stands. Forests. 2018; 9(10):622. https://doi.org/10.3390/f9100622
Chicago/Turabian StylePiotti, Andrea, Matteo Garbarino, Camilla Avanzi, Roberta Berretti, Renzo Motta, Paolo Piovani, and Stefano Leonardi. 2018. "Influence of Spatiotemporal Dynamics on the Fine-Scale Spatial Genetic Structure of Differently Managed Picea abies Stands" Forests 9, no. 10: 622. https://doi.org/10.3390/f9100622