Original article
Continuously missing outer rings in woody plants at their distributional margins

https://doi.org/10.1016/j.dendro.2011.10.001Get rights and content

Abstract

Woody plants growing in seasonal climates normally form one growth ring each year. However, under severe stress conditions they may not complete annual wood production all the way down to the root collar resulting in continuously missing outer rings at lower stem sections (CMORs). Here we test whether CMORs occur at different distributional margins of woody plant species, where stress levels are expected to be high. We tested 13 species (202 individuals) of trees and shrubs growing at elevational and latitudinal shrub- and tree-lines, under conditions that are normally associated with a reduction of radial growth such as drought, cold or nutrient deficiency. Samples were collected from Alaska, north western Russia, Central Europe, Scandinavia and south eastern Spain. Annual radial growth was measured along several disks or cores of each individual applying the serial sectioning technique. Individuals of nine species showed CMORs. The proportion of individuals with CMORs within a sampled species and site ranged from 0% to 80%. The number of CMORs within an individual increased with decreasing sampling height on the stem. Significant correlations existed between the amount of CMORs and (i) cambial age, (ii) stem length, (iii) stem proportion/length below peat surface, and (iv) herbivore-caused defoliation intensity depending on the species and sampling location. Our results suggest that CMORs can be associated with a cambium that may be inactive, yet functional, for up to 18 years. We conclude that CMORs can occur in a wide variety of species, growth forms and biomes, suggesting a general strategy of woody plant growth. To avoid miss-dating in dendrochronological studies, we further recommend the use of the serial sectioning technique for woody plants growing in unfavorable environments, above all, when sample size is limited and when no established chronology for cross-dating is available.

Introduction

Sampling of woody material for age determination or other dendrochronological analyses is usually performed at a certain stem height. This sampling height can vary from breast height (1.3–1.4 m), traditionally applied in forestry and dendrochronology, to ground surface in the case of smaller individuals, or even be at the root collar if exact age determination is aimed for. The underlying assumption is that a woody plant growing in a seasonal climate will form one growth ring per year from the tip of the branches to the root collar. This implies that in a living individual, the outermost ring is the growth ring formed in the year of sampling or in the year before sampling if the new growing season has not yet started.

However, there are three types of deviation from this rule: (1) locally missing rings (LMR), where one or more growth rings are missing in some part(s) of the plant; (2) totally missing rings (TMR), where a plant does not produce wood anywhere in a specific year, and (3) continuously missing outer rings at the stem base (CMORs). This means that the last several growth rings of an individual are missing at the stem base or lower portion of the stem, but that they can be present higher up the stem.

LMRs have been frequently reported, generally resulting from drought stress in woody plants (Stokes and Smiley, 1968, Schweingruber, 1996). TMRs have not been reported widely (but see Novak et al., 2011) because it is necessary to analyze several stem and branch disks of a particular woody plant to discover TMRs.

CMORs, on the other hand, have been reported notably from trees growing in suppressed conditions under a closed forest canopy (Niklasson, 2002), from trees with soil accumulation around the lower stem (Peters et al., 2002), which often form adventitious roots (DesRochers and Gagnon, 1997, Parent and Morin, 2002), from (prostrate) shrubs (Kolishchuk, 1990, Hallinger et al., 2010, Hallinger and Wilmking, 2011) or from woody plants affected by combinations of some of these factors (Parent and Morin, 2002). In these cases, simple ring count at stem base or the apparent root collar often did not reveal the true age of an individual (Kneeshaw and Claveau, 2001, Parent and Morin, 2002, Peters et al., 2002, Lieffers and Stadt, 2003, Hallinger et al., 2010). True age could only be determined by additional analyses, such as pith-node counting (Niklasson, 2002) or within-tree-crossdating, also called serial sectioning (Kolishchuk, 1990, DesRochers and Gagnon, 1997, Gutsell and Johnson, 2002, Niklasson, 2002, Bär et al., 2006). Studies have suggested that CMORs are caused either by soil accumulation around the stem or by other limiting environmental factors, e.g. light limitation (Gutsell and Johnson, 2002, Niklasson, 2002). This brings up the question if individual plants growing at their species physiological limit, where adverse growing conditions are expected to be more frequent (Körner, 2003), also show CMORs and whether those are distributed equally between different environments, growth forms and species (broad leaved versus coniferous species). In this study we will explore this question by testing seven tree and six shrub species growing at or near their physiological limits: at high elevations and latitudes, on peatlands and permafrost influenced soils, as well as in semi-arid conditions. Additionally, we introduce and discuss several hypotheses of how the non-formation of growth rings can arise to stimulate further research on this morphological phenomenon.

Section snippets

Shrubs at their elevational limit

Denali National Park, Alaska, USA: at three south-facing slopes in and around Denali National Park we sampled six individuals each of Salix alaxensis (Andersson) Coville, Alnus crispa (Aiton) Pursh and Juniperus nana Wild, as well as five individuals of Betula nana. L. We sampled the individuals of each species at their elevational margin of distribution on south-facing slopes with an inclination of 5–25°. Distance between sampling disks was 20 cm.

Central Europe, Czech Republic: 26 individuals

Results

In total, 202 individuals (92 shrubs and 110 trees) were sampled (Fig. 1, Table 1) and ∼20% of all sampled individuals showed CMORs. Within a single species, the proportion of individuals with CMORs ranged from 0 to 80%. The number of CMORs within an individual generally decreased with increasing sampling height on the stem (e.g. Fig. 3). CMORs occurred in the genera of Betula (shrubs and trees), Juniperus, Salix and Pinus (shrubs and trees), but not in Alnus and Picea. In the following, we

Discussion

Generally, the occurrence of a successively increasing number of missing outer rings within the lower portion of the stems (CMORs) of several shrub and tree species is surprising, since it is generally assumed that woody plants growing in a seasonal climate form every year a ring extending from the tip of the branches to the root collar. Even though our sample size varied a lot (ranging from a single individual to 81 individuals of a species) we found CMORs both in angiosperms and gymnosperms,

Conclusion

We found CMORs in about 20% of our sampled 202 individuals and in eight of 13 species. Sampled woody plants had a wide variety of growth forms and species and they came from very different landscapes and micro-topographic and climatic settings. Their common feature was that all specimens were growing near or at the margins of their distribution and were obviously affected by unfavorable growing conditions, some even suffering additional stress from herbivory. Therefore, we conclude that CMORs

Acknowledgments

Funding was provided by an EU ATANS Grant (Fp6 506004), the German Science Foundation (DFG, WI 2680/1-1) and a Sofja Kovalevskaja Award by the Alexander von Humboldt Foundation and the German Ministry for Education and Research to M. Wilmking. Further funding came from the scholarship program of the German Federal Environmental Foundation (M. Hallinger, 20008/983) and the Swiss Academy of Sciences (SCNAT) to F. Babst. The study in Spain was supported by the Spanish Ministry of Education and

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