The 4-Dimensional Plant: Effects of Wind-Induced Canopy Movement on Light Fluctuations and Photosynthesis

Abstract

Physical perturbation of a plant canopy brought about by wind is a ubiquitous phenomenon and yet its biological importance has often been overlooked. This is partly due to the complexity of the issue at hand: wind-induced movement (or mechanical excitation) is a stochastic process which is difficult to measure and quantify; plant motion is dependent upon canopy architectural features which, until recently, were difficult to accurately represent and model in 3-dimensions; light patterning throughout a canopy is difficult to compute at high-resolutions, especially when confounded by other environmental variables. Recent studies have reinforced the expectation that canopy architecture is a strong determinant of productivity and yield; however, links between the architectural properties of the plant and its mechanical properties, particularly its response to wind, are relatively unknown. As a result, biologically relevant data relating canopy architecture, light- dynamics, and short-scale photosynthetic responses in the canopy setting are scarce. Here, we hypothesize that wind-induced movement will have large consequences for the photosynthetic productivity of our crops due to its influence on light patterning. To address this issue, in this study we combined high resolution 3D reconstructions of a plant canopy with a simple representation of canopy perturbation as a result of wind using solid body rotation in order to explore the potential effects on light patterning, interception, and photosynthetic productivity. We looked at two different scenarios: firstly a constant distortion where a rice canopy was subject to a permanent distortion throughout the whole day; and secondly, a dynamic distortion, where the canopy was distorted in incremental steps between two extremes at set time points in the day. We find that mechanical canopy excitation substantially alters light dynamics; light distribution and modeled canopy carbon gain. We then discuss methods required for accurate modeling of mechanical canopy excitation (here coined the 4-dimensional plant) and some associated biological and applied implications of such techniques. We hypothesize that biomechanical plant properties are a specific adaptation to achieve wind-induced photosynthetic enhancement and we outline how traits facilitating canopy excitation could be used as a route for improving crop yield.

Keywords: canopy; light; mechanical canopy excitation; modelings; movement; photosynthesis; wind.

Figure 1

Overview of solid body rotation distortion method. Following distortion, 3 × 3 canopies were made.

Figure 2

Changing Light Patterns due to simulated Easterly wind. (A) Schematic of plant distortion indicating center of each triangle before and after simulated mechanical canopy excitation, (B) leaf locations analyzed for light patterns given in (C), the selected light patterns over the whole day where black shaded regions indicate a period of higher light intensity in the undistorted orientation (no wind) and red indicates a period of higher light intensity for the distortion corresponding to an easterly wind. N.B. The three grid strata in (C). Correspond to the canopy strata as indicated by the arrows in (B).

Figure 3

Frequency of PPFD values according to the fraction of surface area received at by a whole plant within a canopy at 9:00, 12:00, and 15:00 h. (A) Top layer, (B) middle layer, and (C) bottom layer where black is the undistorted canopy and red is the distortion equivalent to an easterly wind. (D) Percentage difference in the fraction of the total surface area receiving each PPFD value relative to the undistorted state; i.e., positive values indicate a higher surface area of the easterly wind distorted canopy receiving that set level of PPFD and negative values indicate a higher surface area of the undistorted canopy.

Figure 4

Angle distributions relative to vertical, whereby 0 indicates a vertically inclined leaf section and 90 represents horizontally inclined leaf sections. Data are shown for all canopy locations in the central plant of an undistorted canopy (black) vs. a canopy subject to an easterly wind (red) where (A) frequency of different leaf orientations and (B) distribution of individual leaf sections with depth through the canopy from the top.

Figure 5

Changes as a result of dynamic movement at three time points throughout the day and nine canopy locations (A) PPFD, (B) Carbon gain, (C) normalized carbon gain and (D) percentage difference in carbon gain relative to the undistorted state; where each line represents the average of five measurements from adjacent triangles on the same section of leaf; from the top (black line), the middle (dark gray and dashed line), and the bottom of the canopy (light gray line). Normalised carbon gain was calculated as carbon gain per individual location and averaged across the 5 locations in close proximity on the same leaf (i.e., the 5 locations represented by a single line). Data is presented for 3 different locations (i.e., 3 different leaves) per canopy layer. Values approaching 0 indicate the least favorable orientation in terms of carbon gain and 1 indicates the most favorable.