2024/02/13 by Carlos M. Herrera · 1 voice · 2 citations
Agricultural and Biological Sciences · Biochemistry, Genetics and Molecular Biology · #Plant and Biological Electrophysiology Studies #Plant and animal studies #Plant biochemistry and biosynthesis
paper · pdf · doi:10.1002/ecy.4268
openalex publication_date 2024/02/13 · openalex created_date 2024/03/05 · openalex updated_date 2026/07/22
Torrid summers are consubstantial with the Mediterranean-type climate that prevails over most of the Iberian Peninsula (Capel Molina, 1981). Daily maximum temperature >40°C and relative humidity <10% occur frequently during the rainless period of 3–4 months that follows springtime. This long harsh season brings considerable hardship to plants, particularly in lowland and mid-elevation habitats. Annuals spend the summer as seeds, while herbaceous and woody perennials halt vegetative and reproductive activity (Thompson, 2005). During July–August the decaying remains of withered annuals lying on a dusty ground, the marcescent foliage of summer-deciduous shrubs, and a generalized dearth of wild flowers all combine to make brown the predominant hue in many Iberian landscapes. It thus comes as a pleasant surprise when such brownish estival carpet is broken here and there by the yellow glittering flowerheads of the thistle Carlina corymbosa (Asteraceae; Figure 1A). This perennial herb blooms when hardly any others do and is commonly found in roadsides, open oak woodlands, and clearings in evergreen forests and shrublands, exposed during the daytime to a scorching sunshine. But beyond this visually apprehended peculiarity, the truly outstanding natural history singularity of this thistle is only to be revealed by the sense of touch, more specifically by thermal touch, the perception of temperature of objects in contact with the skin. I discovered by chance that pressing a fingertip on the yellow surface of flowerheads during the hottest period of the day conveyed a cool sensation, as if flowerheads were coolish inside. This observation steered me to articulate the rather counterintuitive hypothesis that during the hottest period of the year, precisely at the time of day when ambient temperature is highest, the flowerheads of summer-flowering C. corymbosa thistles have an interior that is cooler than the surrounding air. As shown in what follows, temperature measurements verified this hypothesis. Instrumental tests were conducted in the field on 1–15 August 2021 and 2023 at two southern Iberian C. corymbosa populations growing in open Quercus ilex woodlands of central Sierra Morena (760 m above sea level [asl], Córdoba province, “mid-elevation site” hereafter), and in large clearings of Pinus nigra forests in the Sierra de Cazorla (1410 m asl, Jaén province, “mountain site” hereafter). The two sites were 155 km apart. Results from the two locations were closely similar, so they will be presented together. Paired measurements of temperature inside individual flowerheads and in the air 2 cm away were taken continuously during periods of 2–5 days. One fine type K thermocouple (exposed junction, 0.2 mm probe diameter, RS PRO Reference 110-4482) was inserted perpendicularly into the flat surface of the flowerhead until it reached the receptacle. A second, similar thermocouple was attached to the flowerhead and its tip kept ~2 cm from the flowerhead's surface. (See Figure 1B for setup.) Wires were attached to the flowerhead and held in place with strips of masking tape. Thermocouples were connected to a battery-powered Omega HH520 data logger/thermometer. For each monitored flowerhead, paired temperature measurements (within and outside the flowerhead, Tin and Tout hereafter, Figure 1B) were continuously recorded at either 3-min (2021) or 1-min intervals (2023). Seven different flowerheads were monitored in this way, yielding a cumulative total of 24,519 paired Tin and Tout records totaling 29.3 flowerhead·days of temperature data (1.9–5.9 days of continuous data per flowerhead; all raw temperature measurements are available in Herrera [2023a]). Preliminary measurements indicated that, during daytime, heating of the exposed probe by solar irradiance led to a rise of 0.2–0.8°C in Tout (depending on wind, orientation, and time of day) relative to the air temperature measured with the probe shaded. This effect most likely led to slightly overestimating the thermal deficit inside flowerheads (ΔT = Tin − Tout) during daytime, but the magnitude of such bias was deemed negligible, and no attempt was made at either shading the external probe or correcting Tout values. Thermal monitoring revealed that the interior of C. corymbosa flowerheads was cooler than the immediately surrounding air most of the time. For all monitored flowerheads combined, Tin was lower than Tout in 88.1% of paired measurements (Appendix S1: Figure S1), the median thermal deficit of the interior of flowerheads relative to the air outside was −3.2°C, and the ΔT interquartile range was −4.9 to −1.2°C, revealing that the thermal deficit was substantial (< −5°C) 25% of the time. Continuous thermal monitoring of individual flowerheads over several days revealed that both internal temperature and thermal deficit followed regular diel rhythms, as illustrated by the temperature time series for two representative flowerheads, one from each study locality, shown in Figure 2. Tin was very similar to Tout from early morning through noon, and both temperatures varied in unison over that period. Tin and Tout became dissociated afterward, and a substantial thermal deficit (ΔT) built up that persisted from noon through at least midnight. The largest ΔT values, approaching −10°C on some days, consistently occurred from noon through early afternoon, coincidentally with the period when Tout reached the daily maxima (Figure 2). There also seemed to be a direct relationship between absolute ΔT and maximum air temperature across different days in the life of the same flowerhead, so that in hotter days the absolute ΔT was larger (in Figure 2, upper graph, compare thermal patterns of mild 9–10 August with those of hot 11–14 August). The finding that flowerheads of C. corymbosa undergo a regular diel rhythm of internal refrigeration raises questions about the mechanism permitting these plants to periodically cool their flowers in the torrid weather that prevails during its flowering season, but also on the possible costs and benefits associated with the species' floral thermal biology. Regarding the possible cooling mechanism, reduced solar irradiance inside these flowerheads due to self-shading (Karban et al., 2023) can be safely ruled out, since substantial thermal deficits persisted also for most of the night (Figure 2). The most parsimonious hypothesis is that periodic flowerhead cooling in C. corymbosa was achieved by temporarily enhanced transpiration in the florets and/or receptacle. Weak evaporative cooling has been demonstrated experimentally in flowers of convolvulaceous flowers in a tropical environment, but in that instance the flowers did not reach temperatures lower than the environment (Patiño & Grace, 2002). Cooling by transpiration has been reported for leaves of well-watered plants exposed to sunshine, but actual thermal deficits (i.e., Tin − Tout <0) are infrequent and much smaller than those exhibited by C. corymbosa flowerheads (Cook et al., 2021; Linacre, 1964; Still et al., 2022). The high ambient temperature and low relative humidity faced by C. corymbosa presumably augmented the cooling efficacy of transpiration during the hottest part of the day, leading to the large thermal deficits observed. Strong cooling effects arising from intense water evaporation in dry–hot climates have been long used by human cultures from the Mediterranean Basin, Middle East, and Africa as a chilling technique, in the form of sweating pitchers made of porous clay, which typically achieve temperature drops of 5–20°C relative to the ambient temperature (“botijos” in Spanish; Chemin et al., 2018; Martínez de Azagra & Del Río, 2015; Zubizarreta & Pinto, 1995). I propose that the large thermal deficit found inside C. corymbosa flowerheads at high ambient temperatures was achieved through a “botijo effect.” As suggested by one reviewer (Richard Karban), support for this hypothesized mechanism might be found by comparing the cooling ability of plants differing in their access to water, for example, through experimental manipulation of water availability by differential watering. In addition to the elucidation of the mechanism(s) involved, two striking aspects of the thermal biology of C. corymbosa flowerheads deserve attention from a plant ecological perspective. First, since cooling by transpiration involves increased water loss, that C. corymbosa plants can afford such water drains during the harshest period of the Mediterranean dry season points to physiological features enhancing efficiency in water acquisition, storage, or retention. Second, the flowerhead cooling system was somehow shut off by plants from early morning through noon, only to be started again at the moment of the day when ambient temperature was quickly approaching the daily maximum. This can be construed as an “intelligent response” (sensu Trewavas, 2003, 2017) directed to prospectively keep flowerhead temperature below dangerous levels that could impair pollen and ovule performance as a consequence of heat stress (Chaturvedi et al., 2021; Zinn et al., 2010). Pollen germination, for example, declines steeply at temperatures >30°C (Orueta, 2002; Seymour et al., 2009). Whether the daily restart of the cooling system was triggered by fast-rising temperature or by increasing solar irradiance could be dissected experimentally by comparing the daily course of Tin and Tout in flowerheads exposed to different irradiance levels obtained, for instance, by differential shading. Cooling by transpiration can also have indirect beneficial effects on C. corymbosa reproduction via effects on pollinator visitation. Major pollinators of C. corymbosa are medium-sized and large endothermic bees in the genera Anthophora and Megachile, which could risk overheating while foraging in summer sunshine (Corbet & Huang, 2016; Herrera, 2023b; Johnson et al., 2023). Although bees prefer to probe warmer flowers at low ambient temperatures, their preferences shift to cooler flowers at ambient temperatures above ~30°C (Dyer et al., 2006; Norgate et al., 2010; Shrestha et al., 2018). In the hot Mediterranean summer, C. corymbosa flowerheads cooler than the air could therefore be more attractive to bees and have greater pollination success. This hypothesis can be evaluated by assessing the possible detrimental effects of artificially raised temperatures inside flowerheads (e.g., by the insertion of battery-powered resistors; Herrera & Medrano, 2017) on pollinator visitation rates, visit duration, and pollen removal and deposition. I'm indebted to my son, Carlos A. Herrera, for discussion and interpretations of floral cooling from a devil's advocate, physicist's perspective. Richard Karban and Casper van der Kooi provided useful remarks on the manuscript. The research reported here received no specific grant from any funding agency. The author declares no conflicts of interest. Data (Herrera, 2023a) are available in figshare at https://doi.org/10.6084/m9.figshare.24679545.v1. Appendix S1. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.