Long-Term Impacts of Defoliator Outbreaks on Larch Xylem Structure and Tree-Ring Biomass

Abstract

Defoliator insects are a major disturbance agent in many forests worldwide. During outbreaks, they can strongly reduce photosynthetic carbon uptake and impact tree growth. In the Alps, larch budmoth (Zeiraphera diniana) outbreaks affect European larch (Larix decidua) radial growth over several years. However, immediate and legacy effects on xylem formation, structure, and functionality are still largely unknown. In this study, we aimed at assessing the impact of budmoth defoliations on larch xylem anatomical features and tree-ring structure. Analyses were performed in the Lötschental (Swiss Alps) within (1,900 m a.s.l.) and above (2,200 m a.s.l.) the optimum elevational range of larch budmoth. We investigated variability of xylem anatomical traits along century-long treering series of larch (host) and Norway spruce (non-host) trees. We identified eight outbreaks affecting larch xylem anatomy during the 20 th century, particularly at 1,900 m a.s.l. Tracheid number always showed a higher percent reduction than properties of individual cells. Cell lumen size was slightly reduced in the first 2-3 years of outbreaks, especially in the early part of the ring. The more carbon-demanding cell wall was thinned along the entire ring, but more evidently in the last part. Theoretical tree-ring hydraulic conductivity was reduced for several years (up to 6), mostly due to cell number decrease. Reduced cell wall area and cell number resulted in a strong reduction of the tree-ring biomass, especially in the first year of outbreak. Our study shows that, under carbon source limitations caused by natural defoliation, cell division is more impacted than wall thickening and cell enlargement (the least affected process). Consequences on both xylem hydraulic properties and tree-ring biomass should be considered when assessing long-term defoliator effects on xylem functioning, forest dynamics, and terrestrial carbon cycle.

Manipulating phloem transport affects wood formation but not local nonstructural carbon reserves in an evergreen conifer

“…Interestingly, cell size was not affected here, suggesting that any osmotic (or water status) effect on turgor pressure and subsequently on cell enlargement rate was presumably compensated for by an opposite effect on enlargement duration, as increases in cell division would accelerate the progression of the development. While limitation in carbon supply due to natural defoliation can reduce growth (Fierravanti, Rossi, Kneeshaw, De Grandpré, & Deslauriers, 2019) and cell numbers substantially (Castagneri et al, 2020), we found that the cumulative number of cells formed, thus cell division seems to be regulated by carbon supply more generally (including at elevated carbon supply).…”

“…The one study that explored the effects of carbon supply variation on wood anatomy in Norway spruce saplings showed that carbon supply did positively relate to the number of cells formed and lumen diameter, but negatively to cell‐wall thickness in latewood (Winkler & Oberhuber, 2017). Defoliation studies support the positive relation of carbon supply with cell numbers, but showed no clear effect of reduced carbon supply on cell size and/or cell‐wall deposition (Castagneri et al, 2020; Deslauriers, Caron, & Rossi, 2015; Rossi, Simard, Deslauriers, & Morin, 2009), suggesting that the primary effect of carbon supply is on cell numbers. As cell‐wall density is fairly constant (Björklund et al, 2017), the amount of carbon in a growth ring depends primarily on its cumulative cell‐wall area, hence the number of cells and individual cell‐wall areas.…”

Manipulating phloem transport affects wood formation but not nonstructural carbon concentrations in an evergreen conifer

“…Dynamic soluble sugar concentrations have already been argued to drive the early-to-latewood transition (Cartenì et al ., 2018), which is supported by the observed decline in mean cell-wall area at low carbon supply here. While limitation in carbon-supply due to natural defoliation can reduce growth (Fierravanti et al ., 2019) and cell numbers substantially (Castagneri et al ., 2020), we found that the cumulative number of cells formed, thus cell division, and to a smaller degree cell-wall deposition, seem to be regulated by carbon supply more generally (including at elevated carbon supply). Interestingly, cell size was not affected, despite the marked increase in cell number above all phloem transport manipulations, resulting in much higher cumulative cell-wall area, thus biomass.…”

“…Thus, environmental sensitivities of the cambium complicate investigations trying to isolate the influence of carbon supply on wood formation due to differences in environmental conditions in space and time. Nonetheless, cell division, enlargement, and cell-wall deposition have been shown to be affected by changes in carbon status due to natural defoliation (Rossi et al ., 2009; Deslauriers et al ., 2016; Castagneri et al ., 2020). Thus, despite these efforts to quantify the relation between assimilation and growth, the debate on whether carbon supply or demand drive allocation to wood formation is not settled yet (Gessler and Grossiord, 2019).…”

Triggering Bimodal Radial Stem Growth in Pinus sylvestris at a Drought-Prone Site by Manipulating Stem Carbon Availability

“…Below the girdling zone cell differentiation ceased after interruption of C transport by phloem blockage causing a striking decrease in CWT in last few latewood tracheids (resulting in increase of CLD). Although a decrease in CWT in last latewood tracheids frequently occurs (Arzac et al, 2018;Pacheco et al, 2018;Castagneri et al, 2020), a direct link to decline in C availability by girdling can be deduced from observations that (i) cell wall thickening in P. sylvestris lasts until September within the study area (Gruber et al, 2010), (ii) reduction in C supply due to insect defoliation similarly reduces cell wall thickening in conifer species (e.g., Axelson et al, 2014;Castagneri et al, 2020;Peters et al, 2020), and (iii) cell wall thickening has a considerable C requirement (e.g., Cuny et al, 2015).…”