PREMISE OF THE STUDY: A prevailing hypothesis in forest succession is that shade‐tolerant species grow more slowly than shade‐intolerant species, across light conditions, because they prioritize carbon (C) allocation to storage. We examined this hypothesis in a confamilial pair of species, including one of the fastest‐growing tree species in the world ( Eucalyptus globulus ) and a shade‐tolerant, slow‐growing species ( Luma apiculata ). METHODS: Seedlings were subjected to one out of four combinations of light (high vs. low) and initial defoliation (90% defoliated vs. nondefoliated) for four months. Growth, C storage concentration in different organs, leaf shedding, and lateral shoot formation were measured at the end of the experiment. KEY RESULTS: Eucalyptus globulus grew faster than L. apiculata in high light, but not in low light. Both species had lower C storage concentration in low than in high light, but similar C storage concentrations in each light condition. Defoliation had no effect on C storage, except in the case of the old leaves of both species, which showed lower C storage levels in response to defoliation. Across treatments, leaf shedding was 96% higher in E. globulus than in L. apiculata while, in contrast, lateral shoot formation was 87% higher in L. apiculata . CONCLUSIONS: In low light, E. globulus prioritized C storage instead of growth, whereas L. apiculata prioritized growth and lateral branching. Our results suggest that shade tolerance depends on efficient light capture rather than C conservation traits.
Abstract Temperate trees rely on carbon (C) and nutrient remobilization from storage to resume growth after winter. Minimum storage levels during the growing season suggest that remobilization could signify that C availability is insufficient to meet growth demands; consequently, growth might be C and/or nutrient limited. However, it remains unclear whether higher growth demands are covered by higher remobilization. This study examined whether higher C and nutrient demands associated with fast growth or deciduousness rely on greater remobilization. In 11 sympatric deciduous and evergreen angiosperm tree species from southern South America, the magnitude of seasonal remobilization of C and nutrient storage was assessed as the seasonal minimums (relative to seasonal maximums) of whole‐tree non‐structural carbohydrates (NSCs), nitrogen (N) and phosphorus (P) concentrations and pools. The basal area increment and stem wood density were determined for each tree, from which the biomass radial increment (BRI) was estimated. The effects of leaf habit and BRI on the seasonal minimum NSC and nutrient concentrations and pools were analysed using linear mixed effects models. Radial growth was not related to seasonal minimum NSC or nutrient concentrations and pools in either the evergreens or deciduous angiosperms; thus, faster growth was not associated with greater remobilization of C or nutrient stores. Furthermore, larger trees grew faster than smaller ones, but did not have higher remobilization. Deciduous species had higher year‐round whole‐tree NSC and nutrient concentrations than evergreens; however, both groups had similar BRI and seasonal minimum concentrations and pools of NSCs and nutrients. Neither growth rate nor leaf habit drove the magnitude of C and nutrient remobilization in the angiosperm trees examined here, indicating no C or nutrient limitation. This result contradicts the view that growth and storage strongly regulate one another, as proposed by a growth‐storage trade‐off. A free Plain Language Summary can be found within the Supporting Information of this article.
Since growth is more sensitive to drought than photosynthesis, trees inhabiting dry regions are expected to exhibit higher carbohydrate storage and less growth than their conspecifics from more humid regions. However, the same pattern can be the result of different genotypes inhabiting contrasting humidity conditions. To test if reduced growth and high carbohydrate storage are environmentally driven by drought, we examined the growth and non-structural carbohydrate (NSC) concentrations in single-provenance stands of mature trees of Pinus contorta Douglas and Pinus ponderosa Douglas ex C. Lawson planted at contrasting humidity conditions (900 versus 300 mm of annual precipitation) in Patagonia, Chile. Individual tree growth was measured for each species and at each location as mean basal area increment of the last 10 years (BAI10), annual shoot elongation for the period 2011–14, and needle length for 2013 and 2014 cohorts. Additionally, needle, branch, stem sapwood and roots were collected from each sampled tree to determine soluble sugars, starch and total NSC concentrations. The two species showed lower mean BAI10 and 2013 needle length in the dry site; P. ponderosa also had lower annual shoot extension for 2011 and 2014, and lower 2014 needle length, in the dry than in the mesic site. By contrast, NSC concentrations of all woody tissues for both species were either similar or higher in the dry site when compared with the mesic site. Patterns of starch and sugars were substantially different: starch concentrations were similar between sites except for roots of P. ponderosa, which were higher in the dry site, while sugar concentrations of all woody tissues in both species were higher in the dry site. Overall, our study provides evidence that reduced growth along with carbon (C) accumulation is an environmentally driven response to drought. Furthermore, the significant accumulation of low-molecular weight sugars in the dry site is compatible with a prioritized C allocation for osmoregulation. However, since this accumulation did not come at the expense of reduced starch, it is unlikely that growth was limited by C supply in the dry site.
Summary An innovative hypothesis to explain the higher carbon (C) and nitrogen (N) storage in woody tissues of winter deciduous species as compared to evergreen species is that these storages reflect an adaptation to tolerate herbivory. Support for this hypothesis has been little when manipulative defoliations were partial and/or applied in a single season. Given that repeated defoliations throughout a single season are common in temperate forests and tend to be more severe in deciduous than in evergreen species, we tested this hypothesis considering complete and recurrent defoliation in two sympatric N othofagus species with contrasting foliar habit. In the field, we applied three defoliation intensities for 3 years in naturally coexisting juvenile trees of N othofagus betuloides (evergreen) and N othofagus pumilio (deciduous). Defoliation intensities included complete defoliation (100%) twice during the growing season, partial defoliation (50%) twice during the whole experiment and no defoliation. We evaluated survival, regrowth and C‐ and N‐storage in the leaves, stems and roots of each tree. Complete defoliation caused 100% mortality in N . betuloides after the first year and no mortality in N . pumilio after 3 years; it induced higher C reductions in N . pumilio roots, supported by greater C‐storage. Partial defoliation caused no interspecific differences in survival, though it produced a stronger decrease in C‐storage in N . betuloides than in N . pumilio . N concentrations in woody tissues were significantly higher in N . pumilio than in N . betuloides , and only in the former did they decrease with the defoliation intensity. Synthesis . We found a potential functional link between leaf habit, defoliation tolerance and C‐ and N‐storage. The deciduous species tolerated complete and recurrent defoliations better than the evergreen species, which was associated with higher C‐ and N‐storage in stems and roots of the former. This link was not detected under partial defoliation. We suggest that the higher C‐ and N‐storage in the woody tissues of deciduous species as compared to evergreen species is an adaptation to tolerate complete and recurrent defoliations under which temperate winter deciduous species may have evolved.
Worldwide drought events causing tree growth decline and mortality are altering the carbon (C) balance of forest ecosystems. One unexplored aspect of trees’ vulnerability is whether responses to drought may be linked to species’ niche breadth. Using the most severe 2015-2016 El Niño drought event in the last 70 years in Patagonia, we determined pre- and post-drought growth, C reserves, wood isotopes, and vessel diameter in eight angiosperm tree species of contrasting niche breadth across a sharp precipitation gradient in southern Chile. All species responded in unison after the drought with a non-water-conservative response, maintaining growth and C reserves, decreasing δ13C, and increasing both vessel diameter and the soluble sugars:starch ratio relative to pre-drought. We unequivocally showed a functional coordination of organisms’ vital traits, a drought-induced acclimation based on starch conversion into soluble sugars in all of the tree species we examined, regardless of their niche breadth and habitat preference.
A long-running debate centres on whether shade tolerance of tree seedlings is mainly a function of traits maximizing net carbon gain in low light, or of traits minimizing carbon loss. To test these alternatives, leaf display, light-interception efficiency, and simulated net daily carbon gain of juvenile temperate evergreens of differing shade tolerance were measured, and how these variables are influenced by ontogeny was queried.
Background and Aims There is a growing concern about how forests will respond to increased herbivory associated with climate change. Carbon (C) and nitrogen (N) limitation are hypothesized to cause decreasing growth after defoliation, and eventually mortality. This study examines the effects of a natural and massive defoliation by an insect on mature trees' C and N storage, which have rarely been studied together, particularly in winter-deciduous species. Methods Survival, growth rate, carbon [C, as non-structural carbohydrate (NSC) concentration] and nitrogen (N) storage, defences (tannins and total polyphenols), and re-foliation traits were examined in naturally defoliated and non-defoliated adult trees of the winter-deciduous temperate species Nothofagus pumilio 1 and 2 years after a massive and complete defoliation caused by the caterpillar of Ormiscodes amphimone (Saturniidae) during summer 2009 in Patagonia. Key Results Defoliated trees did not die but grew significantly less than non-defoliated trees for at least 2 years after defoliation. One year after defoliation, defoliated trees had similar NSC and N concentrations in woody tissues, higher polyphenol concentrations and lower re-foliation than non-defoliated trees. In the second year, however, NSC concentrations in branches were significantly higher in defoliated trees while differences in polyphenols and re-foliation disappeared and decreased, respectively. Conclusions The significant reduction in growth following defoliation was not caused by insufficient C or N availability, as frequently assumed; instead, it was probably due to growth limitations due to factors other than C or N, or to preventative C allocation to storage. This study shows an integrative approach to evaluating plant growth limitations in response to disturbance, by examining major resources other than C (e.g. N), and other C sinks besides storage and growth (e.g. defences and re-foliation).
Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g−1 for soluble sugars, 6–533 (mean = 94) mg g−1 for starch and 53–649 (mean = 153) mg g−1 for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R2 = 0.05–0.12 for soluble sugars, 0.10–0.33 for starch and 0.01–0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g−1 for total NSC, compared with the range of laboratory estimates of 596 mg g−1. Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41–0.91), but less so for total NSC (r = 0.45–0.84) and soluble sugars (r = 0.11–0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods.
Climate change may lead to C stress (negative C balance) in trees. Because nonstructural carbohydrates (NSC) are required during metabolic reactivation in the spring, C stress might delay budbreak timing. This effect is expected to be greater in shade-intolerant than in shade-tolerant species, owing to the faster C economy in the shade-intolerant.We experimentally induced C stress in saplings of six temperate tree species that differed in their light requirements by exposing them to either full light or shade from summer to spring, then recorded the date of first budbreak for the individuals. Because the levels of C reserves that represent effective C stress may differ among species, we estimated the degree of C stress by recording survival during the experiment and measuring whole-sapling NSC concentrations after budbreak.Shade reduced NSC concentrations and increased the sugar fraction in the NSC in all species. In the shade, shade-intolerant species had higher mortality and generally lower NSC concentrations than the shade-tolerant species, indicating a trend for more severe C stress in species with faster C economy. In shade-intolerant species, budbreak started earlier and proceeded faster in full light than in shade, but in shade-tolerant species budbreak was delayed in full light. The effects of the light environments on budbreak were not greater in shade-intolerant than in shade-tolerant species.Our study reveals a correspondence between budbreak responses to light and the light requirements of the species. This finding confirms that C metabolism has a significant role in triggering budbreak and demonstrates that whether C stress accelerates or delays budbreak depends on the species' light requirements.
Abstract Worldwide drought events have been reported to cause tree growth decline and mortality, thus altering the carbon (C) balance of forest ecosystems. While most of the attention has been focused on the physiological mechanisms associated with drought‐induced tree responses of a few species at specific locations, the ecological attributes of these species, like their niche breadth, may be also important in determining species’ sensitivity or resilience to drought. We postulated that wide‐niche breadth tree species should be more drought‐resilient than narrow‐niche breadth species. Using the most severe 2015–2016 El Niño drought event in the last 70 years in Patagonia, we determined pre‐ and post‐drought growth (BAI, basal area increment), C reserves in the form of non‐structural carbohydrate concentrations (NSCs = starch and soluble sugars), wood isotope (δ 13 C, iWUE and δ 18 O) signalling and xylem anatomy (mean vessel diameter, mvd ) in eight angiosperm tree species of contrasting niche breadth across a sharp precipitation gradient in southern Chile. All species responded in unison after the drought with a non‐water‐conservative response, maintaining BAI and NSCs, decreasing δ 13 C, and increasing both mvd and the soluble sugars:NSCs ratio relative to pre‐drought time. Contrary to previous results reporting species‐specific drought responses, our results show unequivocally a functional coordination of organisms’ vital traits associated with a non‐water‐conservative strategy, and a drought‐induced acclimation based on starch conversion into soluble sugars in all of the tree species we examined, regardless of their niche breadth and habitat preference. We state that abiotic drivers such as drought may have selected similar interspecific responses provided that they operate at the community level rather than at the species level. These findings mark the need to revise current views about the ultimate interspecific functional coordination of organisms’ vital traits when facing more frequent and intensive drought events. A free Plain Language Summary can be found within the Supporting Information of this article.
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