plants Communication Shade Avoidance and Light Foraging of a Clonal Woody Species, Pachysandra terminalis Risa Iwabe, Kohei Koyama * and Riko Komamura Laboratory of Plant Ecology, Department of Agro-Environmental Science, Obihiro University of Agriculture and Veterinary Medicine, Inadacho, Obihiro, Hokkaido 080-8555, Japan * Correspondence: [email protected] Abstract: (1) Background: A central subject in clonal plant ecology is to elucidate the mechanism by which clones forage resources in heterogeneous environments. Compared with studies conducted in laboratories or experimental gardens, studies on light foraging of forest woody clonal plants in their natural habitats are limited. (2) Methods: We investigated wild populations of an evergreen clonal understory shrub, Japanese pachysandra (Pachysandra terminalis Siebold & Zucc.), in two cool-temperate forests in Japan. (3) Results: Similar to the results of herbaceous clonal species, this species formed a dense stand in a relatively well-lit place, and a sparse stand in a shaded place. Higher specific rhizome length (i.e., length per unit mass) in shade resulted in lower ramet population density in shade. The individual leaf area, whole-ramet leaf area, or ramet height did not increase with increased light availability. The number of flower buds per flowering ramet increased as the canopy openness or population density increased. (4) Conclusions: Our results provide the first empirical evidence of shade avoidance and light foraging with morphological plasticity for a clonal woody species. Keywords: clonal plants; clonal species; phalanx; guerrilla; light foraging; phenotypic plasticity; Citation: Iwabe, R.; Koyama, K.; morphology; shade tolerance; shade acclimation; forest understory Komamura, R. Shade Avoidance and Light Foraging of a Clonal Woody Species, Pachysandra terminalis. Plants 2021, 10, 809. https://doi.org/ 1. Introduction 10.3390/plants10040809 Clonal plants produce their offspring via not only sexual reproduction but also asexual Academic Editor: Frank M. Thomas reproduction, in which new individual clones with an identical gene set, called ramets, are generated [1–6]. Elucidating the mechanism by which clones forage resources in Received: 1 April 2021 heterogeneous environments is a central issue in clonal plant ecology [4,5,7–22], plant Accepted: 15 April 2021 growth modeling [23], and their application in vegetation management [17–20,24–31]. Published: 20 April 2021 Additionally, the spatial arrangement of ramets determines the reproductive success of clonal plants; this is because aggregation of ramets that belong to the same genets leads to Publisher’s Note: MDPI stays neutral an increased percentage of geitonogamous self-pollination [6]. with regard to jurisdictional claims in Plants in forests are often shaded by neighboring plants or canopy trees [20,32–39]. published maps and institutional affil- The theory of resource foraging predicts that clonal plants selectively deploy ramets iations. in places where resources are locally abundant [7–12,18,19,21,40,41]. The foraging of favorable resource-rich patches acts as a mechanism of escape from unfavorable patches, including shaded patches [9,12,18]. Avoidance of shade can be achieved at multiple levels [4,19,38]. In shade, clonal plants often increase specific rhizome length (i.e., length Copyright: © 2021 by the authors. per unit mass) [7,18] and elongate their internodes [7,18,38,42] or increase their petiole Licensee MDPI, Basel, Switzerland. length [38,42,43]. These increases in rhizome and petiole length are shade-induced spacer This article is an open access article elongation phenomena [42,44]. To date, several researchers have investigated the resource distributed under the terms and foraging theory by experimentally studying clonal plants [7–9,11,19,38,41,44]. conditions of the Creative Commons Most of the previous studies on resource foraging of clonal plants were performed Attribution (CC BY) license (https:// using plants that were grown in pots or trays [7–9,18,19,24,40,42,44–47] and/or inside labo- creativecommons.org/licenses/by/ ratories or greenhouses [7,8,19,24,45] rather than in their natural habitats. Nevertheless, it 4.0/). Plants 2021, 10, 809. https://doi.org/10.3390/plants10040809 https://www.mdpi.com/journal/plants Plants 2021, 10, 809 2 of 12 Plants 2021, 10, 809 2of12 has been discussed that plants respond to their environment in different ways depending on whether they are grown in pots or in their natural habitats [5,48,49]. Plants in natu- ralhas habitats been discussed experience that plants greater respond fluctuations to their in environment their environment in different compared ways depending with plants thaton whether grow in they pots are or grown in greenhouses in pots or [in32 their,48]. natural Particularly, habitats artificial [5,48,49 shading]. Plants using in natu- shade clothsral habitats or films experience (e.g., [7, greater10,17,18 fluctuations,42,44–47,50 in–54 their]) does environment not produce compared sunflecks with experienced plants bythat plants grow grown in pots in or natural in greenhouses forest understory [32,48]. Particularly, [32,48]. However, artificial compared shading using with shade studies in laboratoriescloths or films or (e.g., gardens, [7,10 studies,17,18,42 on,44 resource–47,50–54 foraging]) does not of wildproduce plants sunflecks in their experienced natural habitats (e.g.,by plants [12,38 grown,41]) are in natural limited. forest Moreover, understory most [32 of,48 the]. However, previous compared studies on with resource studies foraging in oflaboratories clonal plants or gardens, have investigated studies on resource herbaceous foraging [7 of–12 wild,16– plants20,24, in38 their,40–42 natural,44,46 habitats,47] or bam- boo(e.g., [13 [12,15,38], species.41]) are limited. The reproductive Moreover, most biology of the [1, previous29,55–59] studies and resultant on resource genetic foraging structure ofof populations clonal plants [60 have–62] investigated of clonal woody herbaceous species [7 have–12,16 been–20,24 studied,38,40– intensively.42,44,46,47] orHowever, bam- to boo [13,15] species. The reproductive biology [1,29,55–59] and resultant genetic structure the best of our knowledge, no studies have quantitatively investigated light foraging or of populations [60–62] of clonal woody species have been studied intensively. However, to shade avoidance for clonal woody species. Hence, it is unclear whether the theory of light the best of our knowledge, no studies have quantitatively investigated light foraging or foragingshade avoidance can be applied for clonal to woody woody species. clonal Hence,plants init is forest unclear understory whether the vegetation. theory of light foragingJapanese can be pachysandra applied to woody (Pachysandra clonal plants terminalis in forestSiebold understory et Zucc.; vegetation. Buxaceae) is a short- statureJapanese (ramet pachysandra height approximately (Pachysandra 15–35 terminalis cm atSiebold the study et Zucc.; site), Buxaceae)evergreen is woody a short- clonal speciesstature (ramet[63,64] height that propagates approximately using 15–35 horizontal cm at the (plagiotropic) study site), rhizomes evergreen (i.e., woody belowground clonal stems)species [ [6563].,64 Each] that ramet propagates comprises using a horizontal single (usually (plagiotropic) unbranched) rhizomes vertical (i.e., aboveground belowground stem andstems) evergreen [65]. Each leaves ramet with comprises its appearance a single (usually similar unbranched) to an erect vertical herb (Figure aboveground1). This stem species formsand evergreen a dense standleaves in with a relatively its appearance well-lit similar place to (Figure an erect1a) herb and (Figure a sparse1). stand This in species a shaded placeforms (Figure a dense1b). stand It is in a a monoecious relatively well-lit species place with (Figure unisexual1a) and flowers, a sparse and stand the in fruits a shaded are white drupesplace (Figure (Figure1b).1c). It is This a monoecious species is speciesdistributed with unisexualin East Asia flowers, [ 63], and and the it isfruits widely are white used as a grounddrupes (Figure cover plant1c). This in Japan species (pers. is distributed obs.) and in several East Asia other [63 countries], and it is[53 widely,54,66 used–68]. as Reports a byground Jeong cover and plant Kim in [53 Japan] and (pers. Lee obs.)et al. and [54] several clarified other mechanisms countries [53 of,54 shade,66–68 acclimation]. Reports at theby Jeong level ofand an Kim individual [53] and leaf Lee or et al. ramet [54] (e.g., clarified leaf mechanisms photosynthetic of shade traits acclimation and plasticity at in abovegroundthe level of an vertical individual stem leaf length, or ramet etc.), (e.g., which leaf were photosynthetic generally traitsin agreement and plasticity with typicalin aboveground vertical stem length, etc.), which were generally in agreement with typical shade acclimation responses of nonclonal plants. However, the mechanisms of light shade acclimation responses of nonclonal plants. However, the mechanisms of light foraging and shade avoidance by the deployment of new ramets as a clonal plant were foraging and shade avoidance by the deployment of new ramets as a clonal plant were not investigated in these studies. Therefore, in the present study, we investigated a forest not investigated in these studies. Therefore, in the present study, we investigated a forest woodywoody clonal plant plant that that grows grows in in its its natural