Size‐mediated ageing reduces vigour in trees

Abstract

There is increasing interest in understanding the costs and benefits of increased size and prolonged lifespan for plants. Some species of trees can grow more than 100 m in height and can live for several millennia, however whether these achievements are obtained at the cost of some other physiological functions is currently unclear. As increases in size are usually associated with ageing, it is also unclear whether observed reductions in growth rates and increased mortality rates are a function of size or of age per se. One theory proposes that reduced growth after the start of the reproductive phase is caused by cellular senescence. A second set of theories has focussed instead on plant size and the increased respiratory burdens or excessive height. We report on experimental manipulations to separate the effects of extrinsic factors such as size from those of intrinsic factors such as age for four tree species of contrasting phylogeny and life history. For each species, we measured growth, gas exchange and leaf biochemical properties for trees of different ages and sizes in the field and on propagated material obtained from the same genetic individuals but now all of small similar size in our common gardens. For all species, evidence indicated that size, not cellular senescence, accounted for the observed age-related declines in relative growth rates and net assimilation rates. Two species exhibited evidence of genetic control on leaf characters such as specific leaf area, although size also exerted an independent, and stronger, effect. We found partial support for the theory of hydraulic limitations to tree growth. The lack of a marked separation of soma and germline, an unlimited proliferation potential of meristem cells and the exponential increase in reproductive effort with size all help explain the lack of a senescence-induced decline in trees. It is possible that trees much older than the ones we sampled exhibit senescence symptoms.

Indicadores del decaimiento en bosques de Nothofagus pumilio en el norte de la Patagonia, Argentina

“…Finalmente, dado que el tamaño de los árboles puede condicionar la predisposición al decaimiento, la variable diámetro a la altura del pecho (dap) también fue considerada en los análisis (Mencuccini et al, 2005;Bigler, 2016).…”

Relationships Between Tree Height and Carbon Isotope Discrimination

“…Gas exchange characteristics may change as trees become larger due to sizedependent variation in environmental and structural factors and their interactions, such as changes in light availability, hydraulic conductance, and carbon allocation (e.g., Yoder et al 1994;Gower et al 1996;Ryan and Yoder 1997). Some traits, such as leaf mass per area and sexual maturation, vary with meristem age independently of size (Bond 2000;Bond et al 2007;Greenwood et al 2008;Thomas 2011); however, developmental changes in gas exchange are driven by tree size rather than age (Day et al 2002;Mencuccini et al 2005;Bond et al 2007;Steppe et al 2011). Thus, we use the term size rather than age throughout this paper (McDowell et al 2005).…”

Rate of tree carbon accumulation increases continuously with tree size

“…Thus, large, old trees do not act simply as senescent carbon reservoirs but actively fix large amounts of carbon compared to smaller trees; at the extreme, a single big tree can add the same amount of carbon to the forest within a year as is contained in an entire mid-sized tree. The apparent paradoxes of individual tree growth increasing with tree size despite declining leaf-level [8][9][10] and stand-level 10 productivity can be explained, respectively, by increases in a tree's total leaf area that outpace declines in productivity per unit of leaf area and, among other factors, age-related reductions in population density. Our results resolve conflicting assumptions about the nature of tree growth, inform efforts to undertand and model forest carbon dynamics, and have additional implications for theories of resource allocation 11 and plant senescence 12 .…”

“…Although the results of a few single-species studies have been consistent with this assumption 15 , the bulk of evidence cited in support of declining growth is not based on measurements of individual tree mass growth. Instead, much of the cited evidence documents either the well-known age-related decline in net primary productivity (hereafter 'productivity') of even-aged forest stands 10 (in which the trees are all of a similar age) or size-related declines in the rate of mass gain per unit leaf area (or unit leaf mass) [8][9][10] , with the implicit assumption that declines at these scales must also apply at the scale of the individual tree. Declining tree growth is also sometimes inferred from life-history theory to be a necessary corollary of increasing resource allocation to reproduction 11,16 .…”

“…First, although growth efficiency (tree mass growth per unit leaf area or leaf mass) often declines with increasing tree size [8][9][10] , empirical observations and metabolic scaling theory both indicate that, on average, total tree leaf mass increases as the square of trunk diameter 17,18 . A typical tree that experiences a tenfold increase in diameter will therefore undergo a roughly 100-fold increase in total leaf mass and a 50-100-fold Table 1.…”