Climate lags and genetics determine phenology in quaking aspen (Populus tremuloides)

Blonder, Benjamin W.; Brodrick, Philip G.; Chadwick, K. Dana; Carroll, Erin; Cruz‐de Hoyos, Roxanne M.; Expósito‐Alonso, Moisés; Hateley, Shannon; Moon, Minkyu; Ray, Courtenay A.; Tran, Hoang; Walton, James A.

doi:10.1111/nph.18850

Climate lags and genetics determine phenology in quaking aspen (Populus tremuloides)

Journal Article · Wed Mar 01 00:00:00 EST 2023 · New Phytologist

DOI:https://doi.org/10.1111/nph.18850· OSTI ID:2998784

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University of California, Berkeley, CA (United States); Rocky Mountain Biological Laboratory, Crested Butte, CO (United States)
California Institute of Technology (CalTech), Pasadena, CA (United States). Jet Propulsion Laboratory (JPL)
Carnegie Inst. of Science, Stanford, CA (United States)
Boston University, MA (United States)
Princeton University, NJ (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Utah State University, Logan, UT (United States)

Spatiotemporal patterns of phenology may be affected by mosaics of environmental and genetic variation. Environmental drivers may have temporally lagged impacts, but patterns and mechanisms remain poorly known. Here, we combine multiple genomic, remotely sensed, and physically modeled datasets to determine the spatiotemporal patterns and drivers of canopy phenology in quaking aspen, a widespread clonal dioecious tree species with diploid and triploid cytotypes. We show that over 391 km² of southwestern Colorado: greenup date, greendown date, and growing season length vary by weeks and differ across sexes, cytotypes, and genotypes; phenology has high phenotypic plasticity and heritabilities of 31–61% (interquartile range); and snowmelt date, soil moisture, and air temperature predict phenology, at temporal lags of up to 3 yr. Our study shows that lagged environmental effects are needed to explain phenological variation and that the effect of cytotype on phenology is obscured by its correlation with topography. Phenological patterns are consistent with responses to multiyear accumulation of carbon deficit or hydraulic damage.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDA; USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2998784

Report Number(s):: PNNL-SA--182758

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 6 Vol. 238; ISSN 0028-646X; ISSN 1469-8137

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (105)

Two-sided confidence intervals for the single proportion: comparison of seven methods Newcombe, Robert G. Statistics in Medicine, Vol. 17, Issue 8 https://doi.org/10.1002/(SICI)1097-0258(19980430)17:8<857::AID-SIM777>3.0.CO;2-E	journal	April 1998
Cytotype and genotype predict mortality and recruitment in Colorado quaking aspen ( Populus tremuloides ) Blonder, Benjamin; Ray, Courtenay A.; Walton, James A. Ecological Applications, Vol. 31, Issue 8 https://doi.org/10.1002/eap.2438	journal	September 2021
Assisted migration is plausible for a boreal tree species under climate change: A quantitative and population genetics study of trembling aspen (Populus tremuloidesMichx.) in western Canada Ding, Chen; Brouard, Jean S. Ecology and Evolution, Vol. 12, Issue 10 https://doi.org/10.1002/ece3.9384	journal	October 2022
Legacy effects of drought in the southwestern United States: A multi-species synthesis Peltier, Drew M. P.; Fell, Michael; Ogle, Kiona Ecological Monographs, Vol. 86, Issue 3 https://doi.org/10.1002/ecm.1219	journal	August 2016
Emerging opportunities and challenges in phenology: a review Tang, Jianwu; Körner, Christian; Muraoka, Hiroyuki Ecosphere, Vol. 7, Issue 8 https://doi.org/10.1002/ecs2.1436	journal	August 2016
Decline in the strength of genetic controls on aspen environmental responses from seasonal to century‐long phenomena Drobyshev, I.; Picq, S.; Ganivet, E. Ecosphere, Vol. 10, Issue 9 https://doi.org/10.1002/ecs2.2869	journal	September 2019
Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae)> Cipollini, Martin L.; Whigham, Dennis F. American Journal of Botany, Vol. 81, Issue 1 https://doi.org/10.1002/j.1537-2197.1994.tb15410.x	journal	January 1994
Development of gridded surface meteorological data for ecological applications and modelling Abatzoglou, John T. International Journal of Climatology, Vol. 33, Issue 1 https://doi.org/10.1002/joc.3413	journal	December 2011
Coping with environmental constraints: Geographically divergent adaptive evolution and germination plasticity in the transcontinentalPopulus tremuloides Goessen, Roos; Isabel, Nathalie; Wehenkel, Christian PLANTS, PEOPLE, PLANET, Vol. 4, Issue 6 https://doi.org/10.1002/ppp3.10297	journal	July 2022
Intersexual differences in phenology and damage by herbivores and pathogens in dioecious Rubus chamaemorus L. Ågren, J. Oecologia, Vol. 72, Issue 2 https://doi.org/10.1007/BF00379262	journal	May 1987
Drought-deciduous behavior reduces nutrient losses from temperate deciduous trees under severe drought Marchin, Renée; Zeng, Hainian; Hoffmann, William Oecologia, Vol. 163, Issue 4 https://doi.org/10.1007/s00442-010-1614-4	journal	April 2010
Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species Vitasse, Yann; Hoch, Günter; Randin, Christophe F. Oecologia, Vol. 171, Issue 3 https://doi.org/10.1007/s00442-012-2580-9	journal	January 2013
The use of digital morphometrics and spring phenology for clone recognition in trembling aspen (populus tremuloides michx.) and its comparison to microsatellite markers Jelínková, Hana; Tremblay, Francine; DesRochers, Annie Trees, Vol. 28, Issue 2 https://doi.org/10.1007/s00468-013-0957-y	journal	November 2013
Frost-Associated Defoliation in Populus tremuloides Causes Repeated Growth Reductions Over 185 years Birch, Joseph D.; Chikamoto, Yoshimitsu; DeRose, R. J. Ecosystems, Vol. 26, Issue 4 https://doi.org/10.1007/s10021-022-00799-w	journal	November 2022
Natural phenological variation in aspen (Populus tremula): the SwAsp collection Luquez, Virginia; Hall, David; Albrectsen, Benedicte R. Tree Genetics & Genomes, Vol. 4, Issue 2 https://doi.org/10.1007/s11295-007-0108-y	journal	August 2007
Premature leaf discoloration of European deciduous trees is caused by drought and heat in late spring and cold spells in early fall Bigler, Christof; Vitasse, Yann Agricultural and Forest Meteorology, Vol. 307 https://doi.org/10.1016/j.agrformet.2021.108492	journal	September 2021
Earlier snowmelt predominates advanced spring vegetation greenup in Alaska Zheng, Jiangshan; Jia, Gensuo; Xu, Xiyan Agricultural and Forest Meteorology, Vol. 315 https://doi.org/10.1016/j.agrformet.2022.108828	journal	March 2022
GCTA: A Tool for Genome-wide Complex Trait Analysis Yang, Jian; Lee, S. Hong; Goddard, Michael E. The American Journal of Human Genetics, Vol. 88, Issue 1 https://doi.org/10.1016/j.ajhg.2010.11.011	journal	January 2011
Phenology and climate relationships in aspen ( Populus tremuloides Michx.) forest and woodland communities of southwestern Colorado Meier, Gretchen A.; Brown, Jesslyn F.; Evelsizer, Ross J. Ecological Indicators, Vol. 48 https://doi.org/10.1016/j.ecolind.2014.05.033	journal	January 2015
Rapid mortality of Populus tremuloides in southwestern Colorado, USA Worrall, James J.; Egeland, Leanne; Eager, Thomas Forest Ecology and Management, Vol. 255, Issue 3-4 https://doi.org/10.1016/j.foreco.2007.09.071	journal	March 2008
Patterns and consequences of ungulate herbivory on aspen in western North America Seager, S. Trent; Eisenberg, Cristina; St. Clair, Samuel B. Forest Ecology and Management, Vol. 299 https://doi.org/10.1016/j.foreco.2013.02.017	journal	July 2013
Tamm Review: Seedling-based ecology, management, and restoration in aspen (Populus tremuloides) Landhäusser, Simon M.; Pinno, Bradley D.; Mock, Karen E. Forest Ecology and Management, Vol. 432 https://doi.org/10.1016/j.foreco.2018.09.024	journal	January 2019
Late snowmelt delays plant development and results in lower reproductive success in the High Arctic Cooper, Elisabeth J.; Dullinger, Stefan; Semenchuk, Philipp Plant Science, Vol. 180, Issue 1 https://doi.org/10.1016/j.plantsci.2010.09.005	journal	January 2011
Continental-scale land surface phenology from harmonized Landsat 8 and Sentinel-2 imagery Bolton, Douglas K.; Gray, Josh M.; Melaas, Eli K. Remote Sensing of Environment, Vol. 240 https://doi.org/10.1016/j.rse.2020.111685	journal	April 2020
Shifting plant phenology in response to global change Cleland, E.; Chuine, I.; Menzel, A. Trends in Ecology & Evolution, Vol. 22, Issue 7 https://doi.org/10.1016/j.tree.2007.04.003	journal	July 2007
Scale gaps in landscape phenology: challenges and opportunities Park, Daniel S.; Newman, Erica A.; Breckheimer, Ian K. Trends in Ecology & Evolution, Vol. 36, Issue 8 https://doi.org/10.1016/j.tree.2021.04.008	journal	August 2021
The multi-institution North American Land Data Assimilation System (NLDAS): Utilizing multiple GCIP products and partners in a continental distributed hydrological modeling system Mitchell, Kenneth E. Journal of Geophysical Research, Vol. 109, Issue D7 https://doi.org/10.1029/2003JD003823	journal	January 2004
Divergent vegetation growth responses to the 2003 heat wave in the Swiss Alps: VEGETATION RESPONSE TO ALPINE HEAT WAVE Jolly, William M.; Dobbertin, Matthias; Zimmermann, Niklaus E. Geophysical Research Letters, Vol. 32, Issue 18 https://doi.org/10.1029/2005GL023252	journal	September 2005
The Community Land Model Version 5: Description of New Features, Benchmarking, and Impact of Forcing Uncertainty Lawrence, David M.; Fisher, Rosie A.; Koven, Charles D. Journal of Advances in Modeling Earth Systems, Vol. 11, Issue 12 https://doi.org/10.1029/2018MS001583	journal	December 2019
Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines Atwell, Susanna; Huang, Yu S.; Vilhjálmsson, Bjarni J. Nature, Vol. 465, Issue 7298 https://doi.org/10.1038/nature08800	journal	March 2010
Net carbon uptake has increased through warming-induced changes in temperate forest phenology Keenan, Trevor F.; Gray, Josh; Friedl, Mark A. Nature Climate Change, Vol. 4, Issue 7 https://doi.org/10.1038/nclimate2253	journal	June 2014
A hydrological simulation dataset of the Upper Colorado River Basin from 1983 to 2019 Tran, Hoang; Zhang, Jun; O’Neill, Mary Michael Scientific Data, Vol. 9, Issue 1 https://doi.org/10.1038/s41597-022-01123-w	journal	January 2022
Sexual homomorphism in dioecious trees: extensive tests fail to detect sexual dimorphism in Populus McKown, Athena D.; Klápště, Jaroslav; Guy, Robert D. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-01893-z	journal	May 2017
Consequences of sexually dimorphic timing of emergence and flowering in Silene latifolia Purrington, Colin B.; Schmitt, Johanna Journal of Ecology, Vol. 86, Issue 3 https://doi.org/10.1046/j.1365-2745.1998.00262.x	journal	June 1998
Costs of Reproduction as Related to the Timing of Phenological Phases in the Dioecious Shrub Pistacia lentiscus L. Milla, R.; Castro-Díez, P.; Maestro-Martínez, M. Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1055/s-2005-872890	journal	January 2006
Variation in leaf flushing date influences autumnal senescence and next year's flushing date in two temperate tree species Fu, Y. S. H.; Campioli, M.; Vitasse, Y. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1321727111	journal	May 2014
Early snowmelt projected to cause population decline in a subalpine plant Campbell, Diane R. Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1820096116	journal	June 2019
The phenology of growth and reproduction in plants Fenner, Michael Perspectives in Plant Ecology, Evolution and Systematics, Vol. 1, Issue 1 https://doi.org/10.1078/1433-8319-00053	journal	January 1998
Regional trends in snowmelt timing for the western United States throughout the MODIS era O’Leary, Donal S.; Hall, Dorothy K.; DiGirolamo, Nicolo E. Physical Geography, Vol. 43, Issue 3 https://doi.org/10.1080/02723646.2020.1854418	journal	December 2020
Changes in duration of reproductive phases and lagged phenological response to experimental climate warming Sherry, Rebecca A.; Zhou, Xuhui; Gu, Shiliang Plant Ecology & Diversity, Vol. 4, Issue 1 https://doi.org/10.1080/17550874.2011.557669	journal	March 2011
Ecological Causes for the Evolution of Sexual Dimorphism: A Review of the Evidence Shine, Richard The Quarterly Review of Biology, Vol. 64, Issue 4 https://doi.org/10.1086/416458	journal	December 1989
Genotypic variation rather than ploidy level determines functional trait expression in a foundation tree species in the presence and absence of environmental stress Eisenring, Michael; Lindroth, Richard L.; Flansburg, Amy Annals of Botany, Vol. 131, Issue 1 https://doi.org/10.1093/aob/mcac071	journal	May 2022
Earlier snowmelt and warming lead to earlier but not necessarily more plant growth Livensperger, Carolyn; Steltzer, Heidi; Darrouzet-Nardi, Anthony AoB Plants, Vol. 8 https://doi.org/10.1093/aobpla/plw021	journal	January 2016
Adaptive capacity in the foundation tree species Populus fremontii: implications for resilience to climate change and non-native species invasion in the American Southwest Hultine, Kevin R.; Allan, Gerard J.; Blasini, Davis Conservation Physiology, Vol. 8, Issue 1 https://doi.org/10.1093/conphys/coaa061	journal	January 2020
Polyploidy: an evolutionary and ecological force in stressful times Van de Peer, Yves; Ashman, Tia-Lynn; Soltis, Pamela S. The Plant Cell, Vol. 33, Issue 1 https://doi.org/10.1093/plcell/koaa015	journal	December 2020
Ontogenetic changes in leaf phenology of Ulmus davidiana var. japonica, a deciduous broad-leaved tree Seiwa, K. Tree Physiology, Vol. 19, Issue 12 https://doi.org/10.1093/treephys/19.12.793	journal	October 1999
Temperature memory and non-structural carbohydrates mediate legacies of a hot drought in trees across the southwestern USA Peltier, Drew M. P.; Guo, Jessica; Nguyen, Phiyen Tree Physiology, Vol. 42, Issue 1 https://doi.org/10.1093/treephys/tpab091	journal	July 2021
Altered leaf morphology, leaf resource dilution and defense chemistry induction in frost-defoliated aspen (Populus tremuloides) St. Clair, S. B.; Monson, S. D.; Smith, E. A. Tree Physiology, Vol. 29, Issue 10 https://doi.org/10.1093/treephys/tpp058	journal	August 2009
Polyploidy influences plant–environment interactions in quaking aspen (Populus tremuloides Michx.) Greer, Burke T.; Still, Christopher; Cullinan, Grace L. Tree Physiology, Vol. 38, Issue 4 https://doi.org/10.1093/treephys/tpx120	journal	September 2017
Intraspecific differences in spring leaf phenology in relation to tree size in temperate deciduous trees Osada, Noriyuki; Hiura, Tsutom Tree Physiology, Vol. 39, Issue 5 https://doi.org/10.1093/treephys/tpz011	journal	February 2019
Current and lagged climate affects phenology across diverse taxonomic groups Prather, Rebecca M.; Dalton, Rebecca M.; barr, billy Proceedings of the Royal Society B: Biological Sciences, Vol. 290, Issue 1990 https://doi.org/10.1098/rspb.2022.2181	journal	January 2023
Xylem Embolism in Response to Freeze-Thaw Cycles and Water Stress in Ring-Porous, Diffuse-Porous, and Conifer Species Sperry, John S.; Sullivan, June E. M. Plant Physiology, Vol. 100, Issue 2 https://doi.org/10.1104/pp.100.2.605	journal	October 1992
Stomatal Closure, Basal Leaf Embolism, and Shedding Protect the Hydraulic Integrity of Grape Stems Hochberg, Uri; Windt, Carel W.; Ponomarenko, Alexandre Plant Physiology, Vol. 174, Issue 2 https://doi.org/10.1104/pp.16.01816	journal	March 2017
Leaf Conductance during the Final Season of a Senescing Aspen Branch Kaufmann, Merrill R. Plant Physiology, Vol. 70, Issue 3 https://doi.org/10.1104/pp.70.3.655	journal	September 1982
Multiple strategies for drought survival among woody plant species Pivovaroff, Alexandria L.; Pasquini, Sarah C.; De Guzman, Mark E. Functional Ecology, Vol. 30, Issue 4 https://doi.org/10.1111/1365-2435.12518	journal	August 2015
Frost hardiness vs. growth performance in trembling aspen: an experimental test of assisted migration Schreiber, Stefan G.; Ding, Chen; Hamann, Andreas Journal of Applied Ecology, Vol. 50, Issue 4 https://doi.org/10.1111/1365-2664.12102	journal	May 2013
Detection of individual ploidy levels with genotyping-by-sequencing (GBS) analysis Gompert, Zachariah; Mock, Karen E. Molecular Ecology Resources, Vol. 17, Issue 6 https://doi.org/10.1111/1755-0998.12657	journal	March 2017
Integrating airborne remote sensing and field campaigns for ecology and Earth system science Chadwick, K. Dana; Brodrick, Philip G.; Grant, Kathleen Methods in Ecology and Evolution, Vol. 11, Issue 11 https://doi.org/10.1111/2041-210X.13463	journal	September 2020
Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation Fitzpatrick, Matthew C.; Keller, Stephen R. Ecology Letters, Vol. 18, Issue 1 https://doi.org/10.1111/ele.12376	journal	September 2014
Tree carbon allocation explains forest drought-kill and recovery patterns Trugman, A. T.; Detto, M.; Bartlett, M. K. Ecology Letters, Vol. 21, Issue 10 https://doi.org/10.1111/ele.13136	journal	August 2018
Ghosts of the past: how drought legacy effects shape forest functioning and carbon cycling Kannenberg, Steven A.; Schwalm, Christopher R.; Anderegg, William R. L. Ecology Letters, Vol. 23, Issue 5 https://doi.org/10.1111/ele.13485	journal	March 2020
Drought's legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk Anderegg, William R. L.; Plavcová, Lenka; Anderegg, Leander D. L. Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12100	journal	January 2013
The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models Keenan, Trevor F.; Richardson, Andrew D. Global Change Biology, Vol. 21, Issue 7 https://doi.org/10.1111/gcb.12890	journal	April 2015
Phenological plasticity will not help all species adapt to climate change Duputié, Anne; Rutschmann, Alexis; Ronce, Ophélie Global Change Biology, Vol. 21, Issue 8 https://doi.org/10.1111/gcb.12914	journal	April 2015
Will phenotypic plasticity affecting flowering phenology keep pace with climate change? Richardson, Bryce A.; Chaney, Lindsay; Shaw, Nancy L. Global Change Biology, Vol. 23, Issue 6 https://doi.org/10.1111/gcb.13532	journal	November 2016
Structural overshoot of tree growth with climate variability and the global spectrum of drought‐induced forest dieback Jump, Alistair S.; Ruiz‐Benito, Paloma; Greenwood, Sarah Global Change Biology, Vol. 23, Issue 9 https://doi.org/10.1111/gcb.13636	journal	March 2017
Plant phenology and global climate change: Current progresses and challenges Piao, Shilong; Liu, Qiang; Chen, Anping Global Change Biology, Vol. 25, Issue 6 https://doi.org/10.1111/gcb.14619	journal	April 2019
Testing early warning metrics for drought‐induced tree physiological stress and mortality Anderegg, William R. L.; Anderegg, Leander D. L.; Huang, Cho‐ying Global Change Biology, Vol. 25, Issue 7 https://doi.org/10.1111/gcb.14655	journal	May 2019
Remote sensing of cytotype and its consequences for canopy damage in quaking aspen Blonder, Benjamin; Brodrick, Philip G.; Walton, James A. Global Change Biology, Vol. 28, Issue 7 https://doi.org/10.1111/gcb.16064	journal	January 2022
No evidence for a negative effect of growing season photosynthesis on leaf senescence timing Lu, Xinchen; Keenan, Trevor F. Global Change Biology, Vol. 28, Issue 9 https://doi.org/10.1111/gcb.16104	journal	February 2022
Clonal dynamics in western North American aspen ( Populus tremuloides ) Mock, K. E.; Rowe, C. A.; Hooten, M. B. Molecular Ecology, Vol. 17, Issue 22 https://doi.org/10.1111/j.1365-294X.2008.03963.x	journal	November 2008
Polyploidy: genome obesity and its consequences Chen, Z. Jeffrey; Ha, Misook; Soltis, Douglas New Phytologist, Vol. 174, Issue 4 https://doi.org/10.1111/j.1469-8137.2007.02084.x	journal	June 2007
ELEVATIONAL GRADIENTS IN ADULT SEX RATIOS AND SEXUAL DIFFERENTIATION IN VEGETATIVE GROWTH RATES OFPOPULUS TREMULOIDESMICHX. Grant, Michael C.; Mitton, Jeffry B. Evolution, Vol. 33, Issue 3 https://doi.org/10.1111/j.1558-5646.1979.tb04744.x	journal	September 1979
Cytological Studies of Diploid and Triploid Populus Tremula and of Crosses Between them Johnsson, Helge Hereditas, Vol. 26, Issue 3-4 https://doi.org/10.1111/j.1601-5223.1940.tb03241.x	journal	July 2010
Modification of Vegetative Phenology in a Tropical Semi-deciduous Forest by Abnormal Drought and Rain1 Borchert, R.; Rivera, G.; Hagnauer, W. Biotropica, Vol. 34, Issue 1 https://doi.org/10.1111/j.1744-7429.2002.tb00239.x	journal	March 2002
Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa McKown, Athena D.; Guy, Robert D.; Klápště, Jaroslav New Phytologist, Vol. 201, Issue 4 https://doi.org/10.1111/nph.12601	journal	November 2013
Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis Wolfe, Brett T.; Sperry, John S.; Kursar, Thomas A. New Phytologist, Vol. 212, Issue 4 https://doi.org/10.1111/nph.14087	journal	July 2016
A simple PCR-based marker to determine sex in aspen Pakull, B.; Kersten, B.; Lüneburg, J. Plant Biology, Vol. 17, Issue 1 https://doi.org/10.1111/plb.12217	journal	June 2014
Autumn senescence in aspen is not triggered by day length Michelson, Ingrid H.; Ingvarsson, Pär K.; Robinson, Kathryn M. Physiologia Plantarum, Vol. 162, Issue 1 https://doi.org/10.1111/ppl.12593	journal	July 2017
Sex-specific responses to climate change in plants alter population sex ratio and performance Petry, William K.; Soule, Judith D.; Iler, Amy M. Science, Vol. 353, Issue 6294 https://doi.org/10.1126/science.aaf2588	journal	July 2016
Increased growing-season productivity drives earlier autumn leaf senescence in temperate trees Zani, Deborah; Crowther, Thomas W.; Mo, Lidong Science, Vol. 370, Issue 6520 https://doi.org/10.1126/science.abd8911	journal	November 2020
Comment on “Increased growing-season productivity drives earlier autumn leaf senescence in temperate trees” Norby, Richard J. Science, Vol. 371, Issue 6533 https://doi.org/10.1126/science.abg1438	journal	March 2021
Impacts of a regional drought on the productivity, dieback, and biomass of western Canadian aspen forests Hogg, E. H. (Ted); Brandt, J. P.; Michaelian, M. Canadian Journal of Forest Research, Vol. 38, Issue 6 https://doi.org/10.1139/X08-001	journal	June 2008
Quantitative-genetic variation in morphological and physiological traits within a quaking aspen ( Populus tremuloides ) population Kanaga, Megan K.; Ryel, Ronald J.; Mock, Karen E. Canadian Journal of Forest Research, Vol. 38, Issue 6 https://doi.org/10.1139/X08-012	journal	June 2008
Genetic adaptation of aspen (Populus tremuloides) populations to spring risk environments: a novel remote sensing approach Li, Haitao; Wang, Xianli; Hamann, Andreas Canadian Journal of Forest Research, Vol. 40, Issue 11 https://doi.org/10.1139/X10-153	journal	November 2010
Genetic mapping of linkage group XIX and identification of sex-linked SSR markers in a Populus tremula × Populus tremuloides cross Pakull, Birte; Groppe, Katrin; Mecucci, Federica Canadian Journal of Forest Research, Vol. 41, Issue 2 https://doi.org/10.1139/X10-206	journal	February 2011
Leaf phenology as an optimal strategy for carbon gain in plants Kikuzawa, K. Canadian Journal of Botany, Vol. 73, Issue 2 https://doi.org/10.1139/b95-019	journal	February 1995
Microsatellite survey reveals possible link between triploidy and mortality of quaking aspen in Kaibab National Forest, Arizona Dixon, Groves B.; DeWald, Laura E. Canadian Journal of Forest Research, Vol. 45, Issue 10 https://doi.org/10.1139/cjfr-2014-0566	journal	October 2015
White tree rings formed in trembling aspen saplings following experimental defoliation Hogg, E. H.; Hart, M.; Lieffers, V. J. Canadian Journal of Forest Research, Vol. 32, Issue 11 https://doi.org/10.1139/x02-114	journal	November 2002
Secondary insects and diseases contribute to sudden aspen decline in southwestern Colorado, USA Marchetti, Suzanne Bethers; Worrall, James J.; Eager, Thomas Canadian Journal of Forest Research, Vol. 41, Issue 12 https://doi.org/10.1139/x11-106	journal	December 2011
Phenological Patterns of Terrestrial Plants Rathcke, B.; Lacey, E. P. Annual Review of Ecology and Systematics, Vol. 16, Issue 1 https://doi.org/10.1146/annurev.es.16.110185.001143	journal	November 1985
The Potential of Aspen Clonal Forestry in Alberta: Breeding Regions and Estimates of Genetic Gain from Selection Gylander, Tim; Hamann, Andreas; Brouard, Jean S. PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0044303	journal	August 2012
Genetic parameters of growth and adaptive traits in aspen (Populus tremuloides): Implications for tree breeding in a warming world Ding, Chen; Hamann, Andreas; Yang, Rong-Cai PLOS ONE, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pone.0229225	journal	March 2020
Genetic Variation and the Natural History of Quaking Aspen Mitton, Jeffry B.; Grant, Michael C. BioScience, Vol. 46, Issue 1 https://doi.org/10.2307/1312652	journal	January 1996
Inherent Variations in the Response of Aspen to Frost Damage Egeberg, Roger Ecology, Vol. 44, Issue 1 https://doi.org/10.2307/1933192	journal	January 1963
Gender‐Specific Physiology, Carbon Isotope Discrimination, and Habitat Distribution in Boxelder, Acer Negundo Dawson, Todd E.; Ehleringer, James R. Ecology, Vol. 74, Issue 3 https://doi.org/10.2307/1940807	journal	April 1993
Effects of Interannual Climate Variation on Phenology and Growth of Two Alpine Forbs Walker, Marilyn D.; Ingersoll, Richard C.; Webber, Patrick J. Ecology, Vol. 76, Issue 4 https://doi.org/10.2307/1940916	journal	June 1995
Dry Season Leaf Production: An Escape from Herbivory Aide, T. Mitchell Biotropica, Vol. 24, Issue 4 https://doi.org/10.2307/2389016	journal	December 1992
Ecology of Aspen in Gunnison County, Colorado Morgan, M. D. American Midland Naturalist, Vol. 82, Issue 1 https://doi.org/10.2307/2423831	journal	July 1969
The Influence of Subalpine Snowbanks on Vegetation Pattern, Production, and Phenology Canaday, B. B.; Fonda, R. W. Bulletin of the Torrey Botanical Club, Vol. 101, Issue 6 https://doi.org/10.2307/2484957	journal	November 1974
Growth in Male and Female Aspen Clones: A Twenty-Five-Year Longitudinal Study Sakai, Ann K.; Burris, Timothy A. Ecology, Vol. 66, Issue 6 https://doi.org/10.2307/2937388	journal	December 1985
pdp: An R Package for Constructing Partial Dependence Plots Greenwell, Brandon,M. The R Journal, Vol. 9, Issue 1 https://doi.org/10.32614/RJ-2017-016	journal	January 2017
Comparative physiology of allopatric Populus species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens Soolanayakanahally, Raju Y.; Guy, Robert D.; Street, Nathaniel R. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00528	journal	July 2015
Simulating coupled surface–subsurface flows with ParFlow v3.5.0: capabilities, applications, and ongoing development of an open-source, massively parallel, integrated hydrologic model Kuffour, Benjamin N. O.; Engdahl, Nicholas B.; Woodward, Carol S. Geoscientific Model Development, Vol. 13, Issue 3 https://doi.org/10.5194/gmd-13-1373-2020	journal	January 2020
Prevernal Leafing of Aspen in Utah Mountains Cottam, Walter P. Journal of the Arnold Arboretum., Vol. 35, Issue 3 https://doi.org/10.5962/p.185977	journal	January 1954

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