The importance of microenvironment: Opuntia plant growth, form and the response to sunlight
Introduction
Maximizing the receipt of photosynthetically active radiation (PAR) is fundamental for plants, even in environments with ample light such as deserts (Nobel, 1981). Opuntia (Cactaceae) are made up of chains of flattened stem segments (platyopuntias) called cladodes (=pads) that are the primary photosynthetic surface. Plant response to PAR includes taller individuals where surrounding vegetation is higher (Nobel, 1981), etiolation of photosynthetic surfaces (Drezner, 2017a,b) to increase light receipt, and cladode oriention to maximize PAR receipt. Opuntia plants in areas with more east-west sun during their growing season orient their pads disproportionately to those directions (Nobel, 1982a; Drezner, 2017a). Differences in PAR receipt on differently oriented surfaces have been documented in other groups such as in Agave deserti (Woodhouse et al., 1980). Nobel (1982a,b) proposed that Opuntia species exhibit a phototropic response by orienting their flat faces in the optimal direction to maximize PAR receipt for growth. Because PAR cannot pass from one side of the pad to the other, unlike for typical thin leaves of non-succulent plants, orientation is an important determinant of PAR receipt (Nobel, 1982a). PAR values may limit net carbon dioxide uptake even on clear days, which is why studies often show non-random orientations across species and populations (Nobel, 1988). Further, because Opuntia are CAM (Crassulacean Acid Metabolism) photosynthesizers, carbon dioxide uptake occurs at night and the often vertical surfaces of these plants result in PAR receipt below 90% saturation (Geller and Nobel, 1987). The orientation bias that results, identified as the ratio between E-W and N-S orientated pads, has been confirmed in over 20 Opuntia species in North America, South America, Australia, and Asia (Nobel, 1982a; Yeaton et al., 1983; Chang and Kim, 1984; Silverman et al., 1988; Drezner, 2017a).
Nobel's (1982a) rule is general, as it is based on the sun's seasonal trajectory across the sky. However, there is great variation in pad orientation at every site, across species, and on any given plant. For example, two terminal pads were randomly sampled on O. cespitosa plants and only 44% of plants had both pads aligned in the same direction (both N-S or E-W) while 56% had one N-S and one E-W oriented pad (unpublished data from Drezner, 2017a). Ratios are highly variable even at similar latitudes (Nobel, 1982a). E-W to N-S ratios (in E-W dominant populations) vary from 1.08, 1.18, 1.21 at some sites, to 1.93, 2.44 to even 3.34 in others (Nobel, 1982a). In the same region in Brazil, O. inamoena and O. palmadora had ratios of 1.08 (not significant) and 1.42 (P < 0.001) respectively (Nobel, 1982a). Thus, from as few as one quarter to nearly half of all pads were oriented in the opposite direction than expected, based on maximizing PAR during the growing season at that latitude (Nobel, 1982a). Other Opuntia studies also show no statistically detectable orientation bias (Abrahamson and Rubinstein, 1976). While no plant would necessarily be expected to produce all their pads in the same direction as there may be structural, physiological or other restrictions, the large amount of variability across sites, species and individuals raises questions about what determines individual pad orientation. Mountains or other more local factors can shift the orientation bias to maintain maximal PAR receipt (Nobel, 1982a, 1988). In Canada, O. cespitosa (formerly O. humifusa) had more E-W facing pads (as expected by Nobel, 1982a), but a second population only 2 km away where tree coverage was substantive to the east and west had more N-S facing pads (Drezner, 2017a). These limited studies suggest that more local factors (rather than just latitude and seasonality of growth) are important, though little work has been done to quantify how local factors affect the morphological response of these plants.
Vegetative reproduction through pad detachment or pad fragments is common in many Opuntia species (Evans et al., 2004; Adanick and Drezner, in review). While new pad orientation may be constrained by the initial orientation of the detached pad or seedling, successive pads orient to increase PAR receipt, producing a slow phototropic response to light conditions (Nobel, 1982a). Terminal pads of Opuntia mesacantha in Florida indeed oriented relatively parallel to their underlying pad, however, the direction of offset was random, even when considering N-S or E-W pads separately (Drezner, 2017a). The high frequency of pads that still deviate from the latitude-season of growth rule reinforces the importance of local processes (Drezner, 2017a). From previous observations, I suggest that orientation may be determined at the areole or pad scale, where broad generalizations (e.g., site or latitude) only provide general patterns whose great deviations remain largely unexplained. Local influences, such as another pad on the same plant casting shade on an areole or area producing a new pad. Such highly local factors are not well understood, but must contribute to orientation, and the large amount of ‘noise’ in pad orientation datasets (e.g. many pads oriented in a non-ideal direction as predicted for maximum PAR receipt) that do not consider local factors.
It is also uncertain if other factors such as position on the plant constrain orientation. For example, Geller and Nobel (1987) observe that Opuntia echinocarpa stems radiate outwards from the plant base. Maximizing PAR has repercussions for surface temperatures (Gibbs and Patten, 1970; Baskin and Baskin, 1973). Opuntia store heat (16 °C above air temperature has been documented) reaching surface temperatures that would be lethal for some plants (Gates et al., 1968; Baskin and Baskin, 1973). Considering that PAR-maximizing orientations would potentially maximize stem heating also, orientation is not for high temperature amelioration (Nobel, 1982a). Less is known about winter temperatures compared to summer temperatures. The surface temperature gap between sun- and shade-facing sides of Carnegiea gigantea is larger in winter than summer (Drezner, 2011), perhaps related to more direct radiation hitting the upright surface during the low sun angles of the winter season, or the more E-W trajectory of the sun in summer which would reduce N-S differences.
Opuntia respond morphologically to environmental variation resulting in great variability of numerous characteristics, such as pad size and shape, even on the same plant (Hanks and Fairbrothers, 1969; Majure and Ervin, 2008), making this taxon ideal for study. The purpose of this study is to quantify Opuntia spp. response to PAR including local-scale shading (e.g., intra-plant shading and local tree cover) by quantifying pad orientation and tilt. I also quantify alternative factors that may affect orientation including location on the plant (i.e., are pads whorled?), and surface temperature differences across differently oriented faces.
Section snippets
Study site and study species
The Robert E. Ward Nature Preserve (33°54′ N, 117°52′W) in the West Coyote Hills, Fullerton, California (Fig. 1), has a Mediterranean climate and coastal sage scrub vegetation, which is endangered due to human development and disturbance (Roach and Wu, 2014). The site is targeted for residential and commercial development (Roach and Wu, 2014). Opuntia littoralis (Engelm.) Cockerell (Cactaceae), O. oricola Philbr., and O. ficus-indica (L.) Miller are common at the Preserve. National Climate Data
Results
Pad L and W, and surface temperatures to the E, W, NW, NE, SW, and SE, and the derived variables E-W and SW-NE temperature, did not deviate significantly from a normal distribution (P < 0.05). Temperatures on the N and S facing sides of the pads, SE-NW, and the L/W ratio did not significantly deviate from normality following transformation (P < 0.05). S-N temperatures and the other variables (in all 3 datasets) either could not be normalized or are categorical variables.
Pads do not show a
Evidence for local scale response to PAR
Nobel (1982a,b) proposed that pad orientation occurs to maximize solar radiation receipt during the growing season, and orientation bias is determined by regional factors such as latitude, and more locally, factors such as topography. These guidelines only offer a basic prediction of orientation bias. Orientation is highly variable even on single individuals, where all orientations are common (Nobel, 1982a; Drezner, 2017a). I suggest plant response to PAR receipt is strongly controlled by local
Conclusions
PAR is known to be limiting for CO2 uptake even in very high PAR environments such as deserts (Nobel, 1981). Nobel (1982a) suggested broad rules to explain PAR response in Opuntia spp. that relate to the astronomical movements of the sun, but these provide only a course generalization; substantial variations are well documented in many species and populations. I observe that pad orientation is best predicted by local-scale (areole, pad, plant) shade. Indeed, a pad 5 cm away may exert more
Declaration of competing interest
The author declares that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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