Papers on tree growth rate vs. longevity, live fast – die young

Forest carbon sink neutralized by pervasive growth-lifespan trade-offs (Brienen et al. 2020) [OPEN ACCESS]. “Land vegetation is currently taking up large amounts of atmospheric CO₂, possibly due to tree growth stimulation. Extant models predict that this growth stimulation will continue to cause a net carbon uptake this century. However, there are indications that increased growth rates may shorten trees′ lifespan and thus recent increases in forest carbon stocks may be transient due to lagged increases in mortality. Here we show that growth-lifespan trade-offs are indeed near universal, occurring across almost all species and climates. This trade-off is directly linked to faster growth reducing tree lifespan, and not due to covariance with climate or environment. Thus, current tree growth stimulation will, inevitably, result in a lagged increase in canopy tree mortality, as is indeed widely observed, and eventually neutralise carbon gains due to growth stimulation. Results from a strongly data-based forest simulator confirm these expectations. Extant Earth system model projections of global forest carbon sink persistence are likely too optimistic, increasing the need to curb greenhouse gas emissions.” Brienen, R.J.W., Caldwell, L., Duchesne, L. et al. Forest carbon sink neutralized by pervasive growth-lifespan trade-offs. Nat Commun 11, 4241 (2020). https://doi.org/10.1038/s41467-020-17966-z

Limited capacity of tree growth to mitigate the global greenhouse effect under predicted warming (Büntgen et al. 2019) [OPEN ACCESS]. “It is generally accepted that animal heartbeat and lifespan are often inversely correlated, however, the relationship between productivity and longevity has not yet been described for trees growing under industrial and pre-industrial climates. Using 1768 annually resolved and absolutely dated ring width measurement series from living and dead conifers that grew in undisturbed, high-elevation sites in the Spanish Pyrenees and the Russian Altai over the past 2000 years, we test the hypothesis of grow fast—die young. We find maximum tree ages are significantly correlated with slow juvenile growth rates. We conclude, the interdependence between higher stem productivity, faster tree turnover, and shorter carbon residence time, reduces the capacity of forest ecosystems to store carbon under a climate warming-induced stimulation of tree growth at policy-relevant timescales.” Büntgen, U., Krusic, P.J., Piermattei, A. et al. Limited capacity of tree growth to mitigate the global greenhouse effect under predicted warming. Nat Commun 10, 2171 (2019). https://doi.org/10.1038/s41467-019-10174-4

Temporal declines in tree longevity associated with faster lifetime growth rates in boreal forests (Searle & Chen, 2018) [OPEN ACCESS]. “Global change has been linked to significant increases in tree mortality in the world’s forests. Reduced tree longevity through increased growth rates has been suggested as one of the mechanisms responsible for the temporal increases in tree mortality, but this idea has not been directly tested. Here we explicitly defined two testable hypotheses: (i) the probability of ageing driven tree mortality increases with global change and (ii) the mortality probability associated with global change is higher for faster growing trees. To test these hypotheses, we examined the temporal changes of tree mortality probability in 539 permanent sample plots monitored from 1960–2009, with ages greater than 100 years at initial censuses, across the boreal region of Alberta, Canada. As expected, we found an overall temporal increase in tree mortality probability, indicating a loss in tree longevity with global change. We also found that trees with faster lifetime growth rates experienced higher temporal increases in mortality probability compared to slower growing trees. An analysis of the responses of tree mortality probability to increasing atmospheric carbon dioxide and temperature and decreases in water availability indicated that increasing atmospheric carbon dioxide and decreasing water availability were the major drivers of declining longevity. Our results suggest that tree longevity may further decline with the expected increase of atmospheric carbon dioxide and decreasing water availability in the region.” Eric B Searle and Han Y H Chen 2018 Environ. Res. Lett. 13 125003. https://doi.org/10.1088/1748-9326/aaea9e

The longevity of broadleaf deciduous trees in Northern Hemisphere temperate forests: insights from tree-ring series (Di Filippo et al. 2015) [OPEN ACCESS]. “Understanding the factors controlling the expression of longevity in trees is still an outstanding challenge for tree biologists and forest ecologists. We gathered tree-ring data and literature for broadleaf deciduous (BD) temperate trees growing in closed-canopy old-growth (OG) forests in the Northern Hemisphere to explore the role of geographic patterns, climate variability, and growth rates on longevity. Our pan-continental analysis, covering 25 species from 12 genera, showed that 300–400 years can be considered a baseline threshold for maximum tree lifespan in many temperate deciduous forests. Maximum age varies greatly in relation to environmental features, even within the same species. Tree longevity is generally promoted by reduced growth rates across large genetic differences and environmental gradients. We argue that slower growth rates, and the associated smaller size, provide trees with an advantage against biotic and abiotic disturbance agents, supporting the idea that size, not age, is the main constraint to tree longevity. The oldest trees were living most of their life in subordinate canopy conditions and/or within primary forests in cool temperate environments and outside major storm tracks. Very old trees are thus characterized by slow growth and often live in forests with harsh site conditions and infrequent disturbance events that kill much of the trees. Temperature inversely controls the expression of longevity in mesophilous species (Fagus spp.), but its role in Quercus spp. is more complex and warrants further research in disturbance ecology. Biological, ecological, and historical drivers must be considered to understand the constraints imposed to longevity within different forest landscapes.” Alfredo Di Filippo, Neil Pederson, Michele Baliva, Michele Brunetti, Anna Dinella, Keiko Kitamura, Hanns D. Knapp, Bartolomeo Schirone, Gianluca Piovesan (2015). Front. Ecol. Evol., Sec. Paleoecology 3(15 May 2015). https://doi.org/10.3389/fevo.2015.00046

Slow lifelong growth predisposes Populus tremuloides trees to mortality (Ireland et al. 2014) [FULL TEXT]. “Widespread dieback of aspen forests, sometimes called sudden aspen decline, has been observed throughout much of western North America, with the highest mortality rates in the southwestern United States. Recent aspen mortality has been linked to drought stress and elevated temperatures characteristic of conditions expected under climate change, but the role of individual aspen tree growth patterns in contributing to recent tree mortality is less well known. We used tree-ring data to investigate the relationship between an individual aspen tree’s lifetime growth patterns and mortality. Surviving aspen trees had consistently higher average growth rates for at least 100 years than dead trees. Contrary to observations from late successional species, slow initial growth rates were not associated with a longer lifespan in aspen. Aspen trees that died had slower lifetime growth and slower growth at various stages of their lives than those that survived. Differences in average diameter growth between live and dead trees were significant (α = 0.05) across all time periods tested. Our best logistical model of aspen mortality indicates that younger aspen trees with lower recent growth rates and higher frequencies of abrupt growth declines had an increased risk of mortality. Our findings highlight the need for species-specific mortality functions in forest succession models. Size-dependent mortality functions suitable for late successional species may not be appropriate for species with different life history strategies. For some early successional species, like aspen, slow growth at various stages of the tree’s life is associated with increased mortality risk.” Ireland, K.B., Moore, M.M., Fulé, P.Z. et al. Slow lifelong growth predisposes Populus tremuloides trees to mortality. Oecologia 175, 847–859 (2014). https://doi.org/10.1007/s00442-014-2951-5

Extreme longevity in trees: live slow, die old? (Issartel & Coiffard, 2011). “We have examined the extreme longevity displayed by trees in relation to a theory mainly developed in animals, namely, the controversial rate of living (ROL) theory of aging which proposes that longevity is negatively correlated to metabolic rate. Plant metabolism implies respiration and photosynthesis; both are susceptible to negatively impact longevity. The relationship between longevity and metabolism was studied in leaves and stems of several species with the aim of challenging the ROL theory in trees. Leaf and stem life spans were found to be highly correlated to metabolism (R ² = 0.97), and stems displayed a much lower metabolism than leaves. Analysis of covariance (ANCOVA), with metabolism as the covariate, revealed no difference between mean leaf and stem life spans, which would appear to conform to the expectations of the ROL theory. Consequently, the extremely high longevity of trees may be explained by the lower metabolism displayed by the stems. These results clearly reflect different energy allocation and energy expenditure rate strategies between leaves and stems, which may result in different senescence rates (and life spans) in these organs. They also suggest that, in contrast to animals, the ROL theory of aging may apply to woody plants at the organ level, thereby opening a promising new line of research to guide future studies on plant senescence.” Issartel, J., Coiffard, C. Extreme longevity in trees: live slow, die old?. Oecologia 165, 1–5 (2011). https://doi.org/10.1007/s00442-010-1807-x

Will the CO2 fertilization effect in forests be offset by reduced tree longevity? (Bugmann & Bigler, 2010) [FULL TEXT]. “Experimental studies suggest that tree growth is stimulated in a greenhouse atmosphere, leading to faster carbon accumulation (i.e., a higher rate of gap filling). However, higher growth may be coupled with reduced longevity, thus leading to faster carbon release (i.e., a higher rate of gap creation). The net effect of these two counteracting processes is not known. We quantify this net effect on aboveground carbon stocks using a novel combination of data sets and modeling. Data on maximum growth rate and maximum longevity of 141 temperate tree species are used to derive a relationship between growth stimulation and changes in longevity. We employ this relationship to modify the respective parameter values of tree species in a forest succession model and study aboveground biomass in a factorial design of growth stimulation × reduced maximum longevity at multiple sites along a climate gradient from the cold to the dry treeline. The results show that (1) any growth stimulation at the tree level leads to a disproportionately small increase of stand biomass due to negative feedback effects, even in the absence of reduced longevity; (2) a reduction of tree longevity tends to offset the growth-related biomass increase; at the most likely value of reduced longevity, the net effect is very close to zero in most multi- and single-species simulations; and (3) when averaging the response across all sites to mimic a “landscape-level” response, the net effect is close to zero. Thus, it is important to consider ecophysiological responses with their linkage to demographic processes in forest trees if one wishes to avoid erroneous inference at the ecosystem level. We conclude that any CO₂ fertilization effect is quite likely to be offset by an associated reduction in the longevity of forest trees, thus strongly reducing the carbon mitigation potential of temperate forests.” Bugmann, H., Bigler, C. Will the CO₂ fertilization effect in forests be offset by reduced tree longevity?. Oecologia 165, 533–544 (2011). https://doi.org/10.1007/s00442-010-1837-4

Functional traits and the growth–mortality trade-off in tropical trees (Wright et al. 2010) [FULL TEXT]. “A trade-off between growth and mortality rates characterizes tree species in closed canopy forests. This trade-off is maintained by inherent differences among species and spatial variation in light availability caused by canopy-opening disturbances. We evaluated conditions under which the trade-off is expressed and relationships with four key functional traits for 103 tree species from Barro Colorado Island, Panama. The trade-off is strongest for saplings for growth rates of the fastest growing individuals and mortality rates of the slowest growing individuals (r² = 0.69), intermediate for saplings for average growth rates and overall mortality rates (r² = 0.46), and much weaker for large trees (r² ≤ 0.10). This parallels likely levels of spatial variation in light availability, which is greatest for fast- vs. slow-growing saplings and least for large trees with foliage in the forest canopy. Inherent attributes of species contributing to the trade-off include abilities to disperse, acquire resources, grow rapidly, and tolerate shade and other stresses. There is growing interest in the possibility that functional traits might provide insight into such ecological differences and a growing consensus that seed mass (SM), leaf mass per area (LMA), wood density (WD), and maximum height (H_max) are key traits among forest trees. Seed mass, LMA, WD, and H_max are predicted to be small for light-demanding species with rapid growth and mortality and large for shade-tolerant species with slow growth and mortality. Six of these trait–demographic rate predictions were realized for saplings; however, with the exception of WD, the relationships were weak (r² < 0.1 for three and r² < 0.2 for five of the six remaining relationships). The four traits together explained 43–44% of interspecific variation in species positions on the growth–mortality trade-off; however, WD alone accounted for >80% of the explained variation and, after WD was included, LMA and H_max made insignificant contributions. Virtually the full range of values of SM, LMA, and H_max occurred at all positions on the growth–mortality trade-off. Although WD provides a promising start, a successful trait-based ecology of tropical forest trees will require consideration of additional traits.” Wright, S.J., Kitajima, K., Kraft, N.J.B., Reich, P.B., Wright, I.J., Bunker, D.E., Condit, R., Dalling, J.W., Davies, S.J., Díaz, S., Engelbrecht, B.M.J., Harms, K.E., Hubbell, S.P., Marks, C.O., Ruiz-Jaen, M.C., Salvador, C.M. and Zanne, A.E. (2010), Functional traits and the growth–mortality trade-off in tropical trees. Ecology, 91: 3664-3674. https://doi.org/10.1890/09-2335.1

Increased early growth rates decrease longevities of conifers in subalpine forests (Bigler & Veblen, 2009) [FULL TEXT]. “For trees, fast growth rates and large size seem to be a fitness benefit because of increased competitiveness, attainment of reproductive size earlier, reduction of generation times, and increased short-term survival chances. However, fast growth rates and large size entail reduced investment in defenses, lower wood density and mechanical strength, increased hydraulic resistance as well as problems with down-regulation of growth during periods of stress, all of which may decrease tree longevity. In this study, we investigated the relationship between longevity and growth rates of trees and quantified effects of spatial environmental variation (elevation, slope steepness, aspect, soil depth) on tree longevity. Radial growth rates and longevities were determined from tree-ring samples of 161 dead trees from three conifer species in subalpine forests of the Colorado Rocky Mountains (Abies lasiocarpa, Picea engelmannii) and the Swiss Alps (Picea abies). For all three species, we found an apparent tradeoff between growth rate to the age of 50 years and longevity (i.e. fast early growth is associated with decreased longevity). This association was particularly pronounced for larger P. engelmannii and P. abies, which attained canopy size, however, there were also significant effects for smaller P. engelmannii and P. abies. For the more shade-tolerant A. lasiocarpa, tree size did not have any effect. Among the abiotic variables tested only northerly aspect significantly favored longevity of A. lasiocarpa and P. engelmannii. Trees growing on south-facing aspects probably experience greater water deficits leading to premature tree death, and/or shorter life spans may reflect shorter fire intervals on these more xeric aspects. Empirical evidence from other studies has shown that global warming affects growth rates of trees over large spatial and temporal scales. For moist-cool subalpine forests, we hypothesize that the higher growth rates associated with global warming may in turn result in reduced tree longevity and more rapid turnover rates.” Bigler, C. and Veblen, T.T. (2009), Increased early growth rates decrease longevities of conifers in subalpine forests. Oikos, 118: 1130-1138. https://doi.org/10.1111/j.1600-0706.2009.17592.x

Age class, longevity and growth rate relationships: protracted growth increases in old trees in the eastern United States (Johnson & Abrams, 2009) [OPEN ACCESS]. “This study uses data from the International Tree-Ring Data Bank website and tree cores collected in the field to explore growth rate (basal area increment, BAI) relationships across age classes (from young to old) for eight tree species in the eastern US. These species represent a variety of ecological traits and include those in the genera Populus, Quercus, Pinus, Tsuga and Nyssa. We found that most trees in all age classes and species exhibit an increasing BAI throughout their lives. This is particularly unusual for trees in the older age classes that we expected to have declining growth in the later years, as predicted by physiological growth models. There exists an inverse relationship between growth rate and increasing age class. The oldest trees within each species have consistently slow growth throughout their lives, implying an inverse relationship between growth rate and longevity. Younger trees (< 60 years of age) within each species are consistently growing faster than the older trees when they are of the same age resulting from a higher proportion of fast-growing trees in these young age classes. Slow, but increasing, BAI in the oldest trees in recent decades is a continuation of their growth pattern established in previous centuries. The fact that they have not shown a decreasing growth rate in their old age contradicts physiological growth models and may be related to the stimulatory effects of global change phenomenon (climate and land-use history).” Sarah E. Johnson, Marc D. Abrams, Age class, longevity and growth rate relationships: protracted growth increases in old trees in the eastern United States, Tree Physiology, Volume 29, Issue 11, November 2009, Pages 1317–1328, https://doi.org/10.1093/treephys/tpp068

Relationships between radial growth rates and lifespan within North American tree species (Black et al. 2008) [FULL TEXT]. “We conducted a meta-analysis of tree-ring data to quantify relationships between growth and lifespan in 4 North American tree species: Tsuga canadensis, Quercus alba, Pinus ponderosa, and Pseudotsuga menziesii. Data sets were compiled from across the range of each species and included a total of 14 341 measured time series. For each species we calculated the age at which each tree was sampled and pooled all trees into 50-y bins. Within each of these 50-y bins, we calculated mean ring width and mean basal area increment in 50-y intervals according to cambial age. Thus, ring widths formed during the same time period in the trees’ life stage could be compared across trees sampled at increasing ages. In all 4 species the longest-lived trees experienced slower growth rates than trees sampled at relatively young ages. Furthermore, long-lived trees with slow growth rates appear to mix with shorter-lived, fast-growing trees in the same forests. Such a relationship between growth and lifespan within species may be an important component of biodiversity that holds implications for old-growth forest development and long-term management.” Bryan A. Black, Jim J. Colbert & Neil Pederson (2008) Relationships between radial growth rates and lifespan within North American tree species, Écoscience, 15:3, 349-357, https://doi.org/10.2980/15-3-3149