The influence of sampling design on tree‐ring‐based quantification of forest growth

Tree-rings offer one of the few possibilities to empirically quantify and reconstruct forest growth dynamics over years to millennia. Contemporaneously with the growing scientific community employing tree-ring parameters, recent research has suggested that commonly applied sampling designs (i.e. how and which trees are selected for dendrochronological sampling) may introduce considerable biases in quantifications of forest responses to environmental change. To date, a systematic assessment of the consequences of sampling design on dendroecological and-climatological conclusions has not yet been performed. Here, we investigate potential biases by sampling a large population of trees and replicating diverse sampling designs. This is achieved by retroactively subsetting the population and specifically testing for biases emerging for climate reconstruction, growth response to climate variability, long-term growth trends, and quantification of forest productivity. We find that commonly applied sampling designs can impart systematic biases of varying magnitude to any type of tree-ring-based investigations, independent of the total number of samples considered. Quantifications of forest growth and productivity are particularly susceptible to biases, whereas growth responses to short-term climate variability are less affected by the choice of sampling design. The world's most frequently applied sampling design, focusing on dominant trees only, can bias absolute growth rates by up to 459% and trends in excess of 200%. Our findings challenge paradigms, where a subset of samples is typically considered to be representative for the entire population. The only two sampling strategies meeting the requirements for all types of investigations are the (i) sampling of all individuals within a fixed area; and (ii) fully randomized selection of trees. This result advertises the consistent implementation of a widely applicable sampling design to simultaneously reduce uncertainties in tree-ring-based quantifications of forest growth and increase the comparability of datasets beyond individual studies, investigators, laboratories, and geographical boundaries.

[1]  Pieter A. Zuidema,et al.  Detecting evidence for CO2 fertilization from tree ring studies: The potential role of sampling biases , 2012 .

[2]  A. Rigling,et al.  Drought response of five conifer species under contrasting water availability suggests high vulnerability of Norway spruce and European larch , 2013, Global change biology.

[3]  F. Babst,et al.  Continuously missing outer rings in woody plants at their distributional margins , 2012 .

[4]  F. Berninger,et al.  Response of Forest Trees to Increased Atmospheric CO 2 , 2007 .

[5]  A. Koutavas CO2 fertilization and enhanced drought resistance in Greek firs from Cephalonia Island, Greece , 2013, Global change biology.

[6]  Franco Biondi,et al.  COMPARING TREE‐RING CHRONOLOGIES AND REPEATED TIMBER INVENTORIES AS FOREST MONITORING TOOLS , 1999 .

[7]  Steven K. Thompson,et al.  Sampling: Thompson/Sampling 3E , 2012 .

[8]  Jörg Franke,et al.  Spectral biases in tree-ring climate proxies , 2013 .

[9]  K. Briffa,et al.  A Closer Look at Regional Curve Standardization of Tree-Ring Records: Justification of the Need, a Warning of Some Pitfalls, and Suggested Improvements in Its Application , 2011 .

[10]  U. Büntgen,et al.  Updating historical tree-ring records for climate reconstruction , 2010 .

[11]  Philippe Ciais,et al.  Site‐ and species‐specific responses of forest growth to climate across the European continent , 2013 .

[12]  David Frank,et al.  Orbital forcing of tree-ring data , 2012 .

[13]  S. Wang,et al.  Feasibility of High-Density Climate Reconstruction Based on Forest Inventory and Analysis (FIA) Collected Tree-Ring Data , 2013 .

[14]  Andrew M. Liebhold,et al.  1200 years of regular outbreaks in alpine insects , 2007, Proceedings of the Royal Society B: Biological Sciences.

[15]  M. Abrams,et al.  Annual growth rings and the impact of Benlate 50 DF fungicide on citrus trees in seasonally dry tropical plantations of northern Costa Rica , 2006 .

[16]  Xiao Jing Guo,et al.  Unusual forest growth decline in boreal North America covaries with the retreat of Arctic sea ice , 2014, Global change biology.

[17]  J. Peñuelas,et al.  European phenological response to climate change matches the warming pattern , 2006 .

[18]  H. Wanner,et al.  2500 Years of European Climate Variability and Human Susceptibility , 2011, Science.

[19]  E. Nikinmaa,et al.  Above-ground woody carbon sequestration measured from tree rings is coherent with net ecosystem productivity at five eddy-covariance sites. , 2014, The New phytologist.

[20]  J. Pierrat,et al.  Effect of sampling effort on the regional chronology statistics and climate-growth relationships estimation , 2013 .

[21]  O. Phillips,et al.  Detecting trends in tree growth: not so simple. , 2013, Trends in plant science.

[22]  T. Wigley,et al.  On the Average Value of Correlated Time Series, with Applications in Dendroclimatology and Hydrometeorology , 1984 .

[23]  Pascale Weber,et al.  Using a retrospective dynamic competition index to reconstruct forest succession , 2008 .

[24]  E. Zorita,et al.  A noodle, hockey stick, and spaghetti plate: a perspective on high‐resolution paleoclimatology , 2010 .

[25]  O. Phillips,et al.  Tropical forests: Tightening up on tree carbon estimates. , 2012, Nature.

[26]  Edward R. Cook,et al.  The 'segment length curse' in long tree-ring chronology development for palaeoclimatic studies , 1995 .

[27]  M. Stambaugh,et al.  HISTORICAL CO2 GROWTH ENHANCEMENT DECLINES WITH AGE IN QUERCUS AND PINUS , 2006 .

[28]  Edward R. Cook,et al.  Calculating unbiased tree-ring indices for the study of climatic and environmental change , 1997 .

[29]  D. Sarewitz Beware the creeping cracks of bias , 2012, Nature.

[30]  Robert J. Pabst,et al.  Rate of tree carbon accumulation increases continuously with tree size , 2014, Nature.

[31]  Craig G. Lorimer,et al.  A methodology for estimating canopy disturbance frequency and intensity in dense temperate forests , 1989 .

[32]  David Frank,et al.  Climate signal age effects—Evidence from young and old trees in the Swiss Engadin , 2008 .

[33]  P. Jones,et al.  Updated high‐resolution grids of monthly climatic observations – the CRU TS3.10 Dataset , 2014 .

[34]  Edward R. Cook,et al.  Asian Monsoon Failure and Megadrought During the Last Millennium , 2010, Science.

[35]  Ranga B. Myneni,et al.  Recent trends in Inner Asian forest dynamics to temperature and precipitation indicate high sensitivity to climate change , 2012 .

[36]  Nathan J B Kraft,et al.  Warming experiments underpredict plant phenological responses to climate change , 2012, Nature.

[37]  J. Ioannidis Why Most Published Research Findings Are False , 2005, PLoS medicine.

[38]  James S. Clark,et al.  The relationship between growth and mortality for seven co‐occurring tree species in the southern Appalachian Mountains , 2002 .

[39]  D. Frank,et al.  Temperature reconstructions and comparisons with instrumental data from a tree‐ring network for the European Alps , 2005 .

[40]  Fritz H. Schweingruber,et al.  Fennoscandian summers from ad 500: temperature changes on short and long timescales , 1992 .

[41]  Andrew G. Bunn,et al.  A dendrochronology program library in R (dplR) , 2008 .

[42]  J. Wallace,et al.  Coherent region-, species-, and frequency-dependent local climate signals in northern hemisphere tree-ring widths , 2011 .

[43]  E. Davidson,et al.  Estimating parameters of a forest ecosystem C model with measurements of stocks and fluxes as joint constraints , 2010, Oecologia.

[44]  Marco Ferretti Concepts and Design Principles Adopted in the International Cooperative Program on the Assessment and Monitoring of Air Pollution Effects on Forests (ICP Forests) , 2013 .

[45]  O. Bouriaud,et al.  Comparative dendroclimatic study of Scots pine, Norway spruce, and silver fir in the Vrancea Range, Eastern Carpathian Mountains , 2009, Trees.

[46]  S. Seneviratne,et al.  Climate extremes and the carbon cycle , 2013, Nature.

[47]  N. Graham,et al.  Continental-scale temperature variability during the past two millennia , 2013 .

[48]  K. Trenberth,et al.  A Global Dataset of Palmer Drought Severity Index for 1870–2002: Relationship with Soil Moisture and Effects of Surface Warming , 2004 .

[49]  Thomas M. Melvin,et al.  Historical growth rates and changingclimatic sensitivity of boreal conifers , 2004 .

[50]  Jan Esper,et al.  Statistical modelling and RCS detrending methods provide similar estimates of long-term trend in radial growth of common beech in north-eastern France , 2011 .

[51]  R. B. Jackson,et al.  A Large and Persistent Carbon Sink in the World’s Forests , 2011, Science.

[52]  N. Breda,et al.  Is ring width a reliable proxy for stem-biomass increment? A case study in European beech , 2005 .

[53]  B. Commarmot,et al.  Age structure and disturbance dynamics of the relic virgin beech forest Uholka (Ukrainian Carpathians) , 2012 .

[54]  E. Xoplaki,et al.  Long‐term drought severity variations in Morocco , 2007 .

[55]  E. Gutiérrez,et al.  Long tree‐ring chronologies reveal 20th century increases in water‐use efficiency but no enhancement of tree growth at five Iberian pine forests , 2011 .

[56]  C. Urbinati,et al.  AGE‐DEPENDENT TREE‐RING GROWTH RESPONSES TO CLIMATE IN LARIX DECIDUA AND PINUS CEMBRA , 2004 .

[57]  Mary Beth Adams,et al.  Forest carbon sequestration changes in response to timber harvest , 2009 .

[58]  E. Cook,et al.  Adjustment for proxy number and coherence in a large‐scale temperature reconstruction , 2007 .

[59]  M. Hughes,et al.  Bristlecone pine tree rings and volcanic eruptions over the last 5000 yr , 2007, Quaternary Research.

[60]  C. Lorimer,et al.  Crown release as a potential old-growth restoration approach in northern hardwoods. , 1997 .

[61]  N. Pederson,et al.  Relationships between radial growth rates and lifespan within North American tree species , 2008 .

[62]  M. Anand,et al.  A likelihood perspective on tree-ring standardization: eliminating modern sample bias , 2013 .

[63]  Jonathan D. Bakker,et al.  A new, proportional method for reconstructing historical tree diameters , 2005 .

[64]  G. Nabuurs,et al.  First signs of carbon sink saturation in European forest biomass , 2013 .

[65]  D. Frank,et al.  Characterization and climate response patterns of a high-elevation, multi-species tree-ring network in the European Alps , 2005 .

[66]  M. Ninyerola,et al.  Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions , 2008 .

[67]  N. Buchmann,et al.  Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review , 2011 .

[68]  M. Dobbertin,et al.  Response of carbon fluxes to the 2003 heat wave and drought in three mature forests in Switzerland , 2012, Biogeochemistry.

[69]  J. Varner,et al.  Canopy disturbance and tree recruitment over two centuries in a managed longleaf pine landscape , 2008 .

[70]  C. Bigler,et al.  Increased early growth rates decrease longevities of conifers in subalpine forests , 2009 .

[71]  M. Dobbertin,et al.  Tree‐life history prior to death: two fungal root pathogens affect tree‐ring growth differently , 2002 .

[72]  E. Mosley‐Thompson,et al.  High-resolution palaeoclimatology of the last millennium: a review of current status and future prospects , 2009 .

[73]  H. Wanner,et al.  Swiss spring plant phenology 2007: Extremes, a multi‐century perspective, and changes in temperature sensitivity , 2008 .

[74]  K. Briffa,et al.  Reassessing the evidence for tree-growth and inferred temperature change during the Common Era in Yamalia, northwest Siberia , 2013 .

[75]  Julio L. Betancourt,et al.  APPLIED HISTORICAL ECOLOGY: USING THE PAST TO MANAGE FOR THE FUTURE , 1999 .

[76]  O. Bräker,et al.  Climate response in dominant and suppressed spruce trees, Picea abies (L.) Karst., on a subalpine and lower montane site in Switzerland , 2001 .

[77]  M. Hughes,et al.  Recent unprecedented tree-ring growth in bristlecone pine at the highest elevations and possible causes , 2009, Proceedings of the National Academy of Sciences.

[78]  R. Siegwolf,et al.  Carbon Flux and Growth in Mature Deciduous Forest Trees Exposed to Elevated CO2 , 2005, Science.

[79]  Aaron A. Berg,et al.  Tree ring evidence for limited direct CO2 fertilization of forests over the 20th century , 2010 .

[80]  E. Vaganov,et al.  Climatically induced interannual variability in aboveground production in forest-tundra and northern taiga of central Siberia , 2006, Oecologia.

[81]  P. Zuidema,et al.  Lifetime growth patterns and ages of Bolivian rain forest trees obtained by tree ring analysis , 2006 .

[82]  Josep Peñuelas,et al.  Increased water‐use efficiency during the 20th century did not translate into enhanced tree growth , 2011 .

[83]  Robert J. Scholes,et al.  A method for calculating the variance and confidence intervals for tree biomass estimates obtained from allometric equations , 2011 .

[84]  M. Dobbertin,et al.  Potential sampling bias in long-term forest growth trends reconstructed from tree rings: A case study from the Italian Alps , 1998 .

[85]  M. Dobbertin,et al.  Tree growth in Swiss forests between 1995 and 2010 in relation to climate and stand conditions: Recent disturbances matter , 2014 .

[86]  M. Bürgi,et al.  Agrarische Waldnutzungen in der Schweiz 1800–1950. Waldfeldbau, Waldfrüchte und Harz | Agricultural use of forests in Switzerland 1800-1950. Field crops and forestry in alternation, forest fruits and resin , 2003 .

[87]  R. Lindroth,et al.  Rising concentrations of atmospheric CO2 have increased growth in natural stands of quaking aspen (Populus tremuloides) , 2009 .

[88]  G. Scarascia-Mugnozza,et al.  Tree rings from a European beech forest chronosequence are useful for detecting growth trends and carbon sequestration , 2004 .

[89]  F. Lebourgeois,et al.  Long-Term Growth Trends of Trees: Ten Years of Dendrochronological Studies in France , 1996 .

[90]  Edward R. Cook,et al.  El Nino modulations over the past seven centuries , 2013 .

[91]  Yuandong Zhang,et al.  Aboveground carbon stock evaluation with different restoration approaches using tree ring chronosequences in Southwest China , 2012 .

[92]  Craig G. Lorimer,et al.  Predicting tree growth from crown variables in managed northern hardwood stands , 1994 .

[93]  Philippe Ciais,et al.  Terrestrial biosphere model performance for inter‐annual variability of land‐atmosphere CO2 exchange , 2012 .

[94]  J. Linares,et al.  From pattern to process: linking intrinsic water‐use efficiency to drought‐induced forest decline , 2012 .

[95]  Michael Grabner,et al.  Long‐term increases in intrinsic water‐use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand , 2011 .

[96]  E. Cook,et al.  Unusual Southern Hemisphere tree growth patterns induced by changes in the Southern Annular Mode , 2012 .

[97]  Miroslav Svoboda,et al.  Disturbance history of an old-growth sub-alpine Picea abies stand in the Bohemian Forest, Czech Republic , 2012 .

[98]  Claire Alix,et al.  Changes in forest productivity across Alaska consistent with biome shift. , 2011, Ecology letters.

[99]  L. Brubaker,et al.  Long‐Term Trends in Forest Net Primary Productivity: Cascade Mountains, Washington , 1989 .

[100]  P. Bernier,et al.  Testing for a CO2 fertilization effect on growth of Canadian boreal forests , 2011 .

[101]  F. H. Schweingruber,et al.  Reduced sensitivity of recent tree-growth to temperature at high northern latitudes , 1998, Nature.