Heliocaminiform structures: plant organs that function as microgreenhouses

Plant pubescence comes about through unicellular to complex multicellular trichomes (Fig. 1). It is important for temperature modification of flowers in some species but has been studied only in a few (Table 1 rows 12, 30, 35 and below). Floral trichomes have been intimated in restrictive pollinator visitation (Kerner 1878) ) and general plant pubescence in herbivore defence (Levin 1973). Levin (1973) also addresses some aspects of phytogeography and pubescence but does not invoke micrometeorological functionality.

Thick pubescence can heat underlying structures in cool, high-elevation environments by increasing the boundary layer of air adjacent to the leaf and reducing convective heat loss (Meinzer and Goldstein 1985), i.e., the greenhouse effect with trapped air within and differential radiative structures (trichomes) without.

We have not reviewed the wide diversity of proposed functions for which experimental evidence is lacking (UV and irradiation protection, moisture accumulation and retention, differential growth by solar aspect and/or compass direction, and perhaps heat accumulation) for pubescence in Cactaceae (Table 1, row 13). However, two studies (Meier 1995; Miller 1986) have evaluated the impact of pubescence on the thermal dynamics of reproductive structures and the downstream impacts on plant reproductive fitness. In the Andes Miller (1986)  records that species of Puya (Bromeliaceae) from high elevations produce denser pubescence than those occurring at lower elevations. More glabrous (i.e., with less pubescence), low-elevation taxa tended to track ambient temperatures while high-elevation pubescent taxa tended to be warmer than ambient conditions. Unmanipulated plants of Puya hamate maintained temperatures 2–3 °C higher than ambient night-time conditions while those denuded of pubescence did not, indicating insulating properties of the pubescence. Finally, north-facing (warmer) inflorescences had elevated seed production compared to south-facing (cooler) inflorescences, providing a link between temperature and fecundity (Miller 1986) (Table 1, row 12). Meier (1995) recorded temperatures within stems and inflorescences of two High Arctic species of Pedicularis, P. lanata and P. hirsuta (Orobanchacaeae) with respect to the heat available to herbivorous larvae of Olethreutes inquietana (Lepidoptera: Tortricidae) and Gonarcticus arcticus (Diptera: Scathophagidae) living within the stems. She found temperatures excesses of several degrees C, and by removing the pubescence on P. hirsuta found that temperature excesses were reduced and of shorter duration (Table 1, row 30). The thermal dynamics of inflorescences with respect to pubescence have also been studied in two Himalayan taxa. Although the woolly inflorescence of Saussurea medusa (Asteraceae) may be 5.9 °C warmer than ambient air temperatures, it is unlikely to be due to pubescence, but rather the compact architecture of the inflorescence itself (Yang et al. 2008). Removal of pubescence in situ and in controlled conditions had negligible impact on heat retention, and thus Yang et al. (2008)  posited that pubescence functions mostly to repel water and/or to reflect UV light (Table 1, row 9). In the Himalayan mint (Eriophyton wallichii (Lamiaceae)), flowers are covered by densely pubescent leaves. Pubescent control leaves absorb slightly more visible light than experimentally shaved leaves, and consequently are significantly warmer (Peng et al. 2015). Peng et al. (2015) authors also evaluated pollen viability and seed production in control plants and those with experimentally lifted leaves, but from these treatments it is difficult to assess the direct effect of pubescence on fitness (Table 1, row 25). Together those studies in Himalayan taxa suggest that pubescence may be less important than leaf architecture in mediating floral temperatures and heliocaminiform effects.

The idea that pubescent flowers. inflorescences, stems, and bracts function as heliocaminiform “hairy heat traps” to warm floral structures was recognized in willows (Krog 1955; Budel 1957; Kevan 1970; Mølgard 1982; 1989). In Alaska, woolly willow catkins may be 15–25 °C warmer at ambient air temperatures of 0 °C, and removal of pubescence reduces temperatures by about 60% relative to unmanipulated catkins (Krog 1955). In willows, sex-based differences in pubescence create disparities in inflorescence temperature with pistillate catkins having denser pubescence and, on average, being significantly warmer than staminate catkins (Kevan 1989) (Table 1, row 35).

Heliocaminiform flowers and inflorescences are discussed in the review by van der Kooi et al. (2019) who comment on the effects of colour, floral form, cellular features, pubescence, and corolla opening and closing (Fig. 2). More recently, Zhang and Tang (2023) observed thermal images of 18 alpine flowering species and recorded a maximum of 11 °C difference between the center and the edge of some blooms, especially in Asteraceae. Many flowers start their development as hollow buds comprising their calyces and corollas and enclosing the reproductive organs. Our review of the literature has uncovered remarkably few examples of the temperatures within floral buds but many studies (not cited) in which the micrometeorology of ambient conditions, especially air temperatures, in close proximity to budding flowers on trees, shrubs, and herbs have been made. We suggest that greater attention to internal temperatures within immature floral structures may help understandings of the development, maturation, and fertility of the reproductive structures within and to issues of sexual compatibility. It is known that the temperatures of floral reproductive organs can have profound influence on pollen viability, compatibility in fertilization, and stigma receptivity over the period of floral development from early bud to complete anthesis (Distefano et al. 2018 for Citrus clementina flowers allowed to develop in incubators).

As noted above, calyces contribute structurally to the hollow forms of floral buds in many plant species and so, presumably and potentially to heliocaminiform effects. Table 1 lists various taxa of plants in which the flowers produce especially well-developed calyces that continue to enclose the corolla after anthesis as proximally connate sepal(s) or as a symsepalous calyx, sometimes referred to as a syncalyx. The syncalyx of many species of Silene presumably function as microgreenhouses, as shown for two Arctic species (Kevan 2020) (Table 1, row 15). The inflated syncalyces of Physalis spp. become heated in sunny weather with the effect of accelerating growth and maturity of the fruit within (Li et al. 2019) (Table 1, row 37).

The translucent and sometimes achlorophyllous terminal leaves of various plants have been demonstrated to function in UV protection of the reproductive structures within, and to allow the plants to accumulate heat by the greenhouse effect, e.g., bracts of Saussurea velutina (Asteraceae) (Yang and Sun 2009) (Table 1, row 9) and Rheum spp. (Polygonaceae) (Omori and Ohba 1996; Omori et al. 2000; Iwashina et al. 2004; Tsukaya 2002; Song et al. 2013) (Table 1, row 33) at high elevations in the Himalayas. The involucral bracts, well known in many Asteraceae, enclose air spaces that likely become warm and protect the inflorescence within. Similarly, the large leaves of sub-antarctic and high mountain mega-herbs have also been suggested to form air-filled spaces that function as microgreenhouses, heating, and protecting the blossoms developing within (Little et al. 2016; Table 1 rows 4, 6, 8, 9, 33).

Another form of bract is exemplified by the flag leaves that characteristically enclose the developing reproductive structures (flowers and fruiting heads) in Poacaea (Table 1, row 32) at the boot stage (i.e., when the immature inflorescence is enclosed within the bracts) may contribute through the microgreenhouse effect to the rapidity of growth and maturation, but we have found no records of this. The same idea may apply to the papery bract, perhaps an epicalyx, that encloses the floral buds of various Amaryllidaceae, such as the familiar daffodil and narcissus (Table 1, row 2). We also suggest that the spadices that enclose the reproductive organs of many palms (Arecaceae) and the involucral bracts of sedges (Cyperaceae) may function similarly while affording protection (Table 1, row 7 and 18, respectively).

We note that various plants produce hollow fruits with translucent outer walls (pericarps) (Fig. 3). Those that we have examined (i.e Asclepias syriaca (Table 1, row 5), Nigella damascina (Table 1, row 34), and Echinocystis lobata (Table 1, row 17) attain elevated internal temperatures in sunshine, sometimes amazingly high (e.g., in follicles of A. syriaca). There are numerous plant taxa that produce hollow, heliocaminiform fruit and suggest themselves for further study, notably in such important families as Fabaceae (Table 1, row 21), Brassicaceae (Table 1, row 11), Cucurbitaceae (Table 1, row17), some Solanaceae (Table 1, row 37), and a few Ericaceae (Table 1, row 19). Koelreuteria appears to be similar with its inflated capsular fruit with seeds inside but it remains unstudied for the possibility of heliocaminiform function (Table 1, row 36).

We know of no general review of hollowness in fruits and, apart from our preliminary records (Table 1), we have found no records of temperature regimes within them.

Few studies have been made on the physical conditions within hollow galls, even those with obviously translucent walls, as the well-known oak-apple (Connald 1908) (Table 1, row 22). Cynipid wasp larvae inhabit the galls, e.g., Biorhiza pallida in Europe, Amphibolips confluenta in eastern North America, and Atrusca bella in western North America. One of the best studied galls is the goldenrod ball gall induced by the fly, Eurosta solidaginis (Diptera: Tephritidae). It occurs conspicuously on the stems of various species of goldenrod, Solidago spp. (Asteraceae) (Table 1, row 9). Layne Jr. (1991. 1993) notes that the galls, which are thick-walled and probably not translucent, in sunshine can attain temperatures up to 5 °C above ambient air temperatures and do buffer the conditions within in hot summer and cold winter conditions. The pistachio horn gall is induced by aphids, Baizongia pistaciae (Hemiptera: Pemphigidae) on pistachio (Pistacia spp. (Anacardiacea)). The galls are large and inhabited by large numbers of aphids. Martinez (2009) records that the galls buffer the inhabitants from extremely high ambient temperatures and insolational heating (Table 1, row 3). With about 13 000 species of gall-inducing organisms known, it is surprising that so little is recorded about the physical conditions within their homes.

In our initial studies of possible heliocaminiform structures in plants, we were surprised to find no general review in the botanical literature from the mid-19th century until today about the occurrence of hollowness in plant stalks (stems, culms, and so on) and little that pertained to the temperature regimes within them (Fig. 4). Billings and Godfrey (1967) proposed that hollow stems in sub-alpine plants may act as greenhouses and ameliorate gas exchange for photosynthesis, growth, and maturation. Stems of wheat (Triticum aestivum (Poacaea)) are also hollow and provide for ameliorated gas exchange and photosynthesis (Bornemisza-Pauspertl et al. 1984). Eriogonum inflatum (Polygonaceae) has specialized, inflated, zone of the stem which has also been proposed to function similarly (Osmond et al. 1987). Neither of the latter studies includes information on temperature relations. The remarkable hollow stems of Caulanthus spp. (Brassicacaea) have not been studied with respect to their potential for heliocaminiform function (2020 (https://www.youtube.com/watch?v=CVpjLRNo1jc)).

Kevan et al. (2018) present a model for the complex thermodynamic interactions within stems and we have followed up with more intense studies, the results of which are briefly summarized in Table 1. We have been surprised to find that temperatures in insolated and shaded stems of Equisetum spp. do not seem to differ from one another nor much from the surrounding air (Table 1, row 38). We conjecture that rapid evapotranspiration (the stems shrivel rapidly when cut) may offset any heating by heliocaminiform function in sunshine.

Pneumatocysts in Fucus, Macrocsytis, Nereocystis, Sargassum are well-known hollow structures in some brown algae (Phaeophyta) (Fig. 5). They are usually explained as aiding in buoyancy of the photosynthetic lamina. As far as we are aware, temperatures have not been measured in pneumatocysts until now, but ambient and internal temperature regimes probably affect the gas (notably CO₂) within (King 2001; Supratya et al. 2020; Liggan and Marton 2020) (Table 1, row 39). Preliminary results from the coast of Anacortes, WA, USA, show temperatures with the pneumatocysts of bladder wrack (Fucus vesiculosus) and bull kelp (Nereocystis luetkeana) (Fig. 5; Table 1 row 39) were about 4 °C warmer than the ambient air under sunny conditions.

The sporophytes of Sphagnum spp. comprise tiny urns on stalks above the main gameotophyte moss (Fig. 5). Presumably the insolation heats and expands the air within the capsule until the capsule bursts and releases the spores upwards (Table 1 row 40 (Kimmerer (2003:118)). The extent to which this heliocaminiform phenomenon occurs in mosses remains to be studied.

A hollow stipe or pileus, or both is characteristic of some fungi, notably Catherellus and Craterellus, Morchella spp., and other basidiocarp fungi (Fig. 5). Most fungi known to have hollow structures grown in shaded environments so microgreenhouse effects from insolation probably do not apply. The structure of the Nidulariaceae suggests that thermal relations and possibly insolation may play a role in maturation (Table 1 row 42).

Lichens show an amazing array of forms and tolerance to heat and desiccation (Lange 1953, 1954) (Fig. 5). Among foliose and fruticose Cladonia spp. are numerous examples of species that are hollow within, especially within the podetium that supports the ascocarp. Thamnolia spp. (worm or bone lichens), some Hypogymnia spp. (e.g., H. tubulosa the powder-headed tube lichen) and Alectoria spp. are also known to have hollow thalli. Species of Letharia (wolf lichens) may be hollow within the fruticose thalli. Although hollow structures may be common within vegetative and reproductive structures of lichens we know of no review of the subject nor of its functionality in lichen growth and reproduction (Table 1 row 41).

Plants become warmed by a complex of thermal processes (Kevan et al. 2019) involving radiative, conductive, and convectional heating. Apart from the influence of the temperature of the ambient air is the likely contribution of solar electromagnetic radiation (UV-Visible-IR). Some impinging radiation is reflected, some is absorbed and some is transmitted through the tissue (translucence) about which little seems to be known. Absorbed radiation is conducted through the stem’s tissue (laterally and longitudinally). It is lost to the stem tissue by radiation and conduction to the outside and inside (lumen) of hollow structures. Transmitted radiation and/or conducted heat contributes additional energy to the lumen. Within the stem, radiant energy, like impinging solar EMR, can be (a) reflected, (b) absorbed by wall tissue from within, and also absorbed by the moist atmospheric gas in the lumen. The energy absorbed by the internal atmosphere contributes to the thermal environment within the heliocaminiform structure by heat exchange by conduction, convection, and re-radiation. The dynamics of how the thermal environment in hollow stems is generated involves various complex processes that result in the rise in temperature measurable by various thermometric instruments. Heated structures liberate their energy through radiation (measurable as Emissivity), conduction to the surrounding air (or water in the case of aquatic plants), and evapotranspiration. Some of the heat generated within hollow structures is conducted elsewhere in the plant by the liquid in conductive tissues (phloem and xylem), some of the EMR is used in photosynthesis, and thermal energy is used in metabolism.

The additional heat resulting from heliocaminiform processes must positively affect photosynthetic metabolism. That, coupled with the enriched gas mixture within hollow structures (e.g., stems of Mertensia ciliata (Boraginaceae) (Billings and Godfrey 1967), Triticum aestivale (Bornemisza-Pauspertl et al. 1984), and Eriogonum inflatum (Osmond et al. 1987 (and see above and Table 1 row 33) would contribute to speed and extent of growth, maturation, and reproduction. There are many plants with hollow structures, especially stems. Such forms are probably multifunctional and for stems include compressional, torsional, and bending strength (Niklas 1992; Niklas and Spatz 2012) and rapidity of growth, especially in early development. Those features, coupled with capacity for internal heating through heliocaminiform effects, and retention of gases that enhance photosynthetic biochemical reactions illustrate multifunctionality. Although the woody walls of mature stems probably do not allow for heliocaminiform effects, they loft reproductive organs above the canopy, so aiding in pollination and subsequent seed dispersal. An extreme example is the Bambusoideae (Poacaea) spp.), known to include the fasted growing plants on Earth and appreciated for use from salads to scaffolding but we are unaware of any observations on the temperatures or other conditions (e.g.,gaseous) within bamboo culms.

Biothermometry has been applied to plants through direct measurements and by remote IR thermometry. For flowers, the means of warming under cool conditions have been recently reviewed (van der Kooi et al. 2019) and include solar basking by orientation of plant parts to face the sun, closing of leaves or floral parts and so retaining heat, adaptations that emulate translucent miniature greenhouses and, in some special cases, metabolic heating. For other plants parts, notably stems, Kevan et al. (2018) show that hollowness imbues plants with elevated temperatures in sunny conditions. Cooling under heat stress is less understood. Apart from the orientation of leaves by paraheliotropism to reduce solar heating, cooling is attributed to transpirational heat loss (i.e., heat loss by the evaporation of water through stomata, akin to sweating (e.g., Equisetum spp. Table 1, row 38, corn sweat, some fruit and galls). The cooling effect of trees is not simply by shading but includes transpiration and may involve paraheliotropism. Those phenomena are increasingly invoked for mitigation of heat in urban landscapes. Herbaceous plants may also exhibit paraheliotropism and so reduce incident solar heating stress, but, additionally, show growth responses mediated by interacting heat and light sensitivities that result in heat avoidance. Thus, plants, although apparently static and passive, show remarkable capacities to regulate their internal temperatures by a complex variety of strategies. Those include solar heating, as in diaheliotropic solar furnaces (Kevan 1989), microgreenhouse effects (Kevan et al. 2018; Kevan 2019a, 2019b, 2020), metabolic endothermy (van der Kooi et al. 2019) and concomitant cooling by evapotranspiration (as noted above and referred to as the swamp cooler effect (Galen 2006)), paraheliotropism and adaptive morphogenesis (Crawford et al. 2012). Thus, plants, although apparently static and passive, show remarkable capacities to regulate their internal temperatures by a complex variety of strategies. Thus, plants are, as Michaletz et al. (2015) argue, but from the viewpoint of metabolism, limited homoeotherms!

There are increasing amounts of information in the modern scientific literature on the observed effects of climate change on plant distributions and to a lesser extent growth rates (Post 2013) but fewer studies on the micrometeorological basis of concomitant effects in phenological mismatches between plants and their symbionts (other plants, herbivores, mutualists). Recent papers have pointed out the consequences of recently documented phenological mismatches in pollination through pollinator availability and activity and flowering times (Høye et al. 2013; Miller-Struttmann et al. 2015; Wheeler et al. 2015). There have been major advances in micrometeorology and the effects of ambient temperatures, and other factors, on the growth and productivity of plants, especially for agriculture and forestry (Jones 2013). It is acknowledged that intraplant thermal regimes influence reproductive fitness of plants directly through the growth and presentation of the sexual organs (flowers and inflorescences) and indirectly through performance of the vegetative parts. There are surprisingly few studies on how supporting structures (stems, petioles, peduncles, culms etc.) capture and use ambient heat (including solar radiation) to enhance their presentations for pollination (by insects or by wind) or for seed/fruit dispersal (mostly by wind) (Kevan et al. 2018). In short, there appears to be major gaps in knowledge linking climate change with whole plant phenology, vegetative productivity and reproductive fitness. We suggest that studies are urgently needed to better understand the form and function of plant structures in terms of their abilities to develop micrometeorological environments that seem assuredly influenced by climate changes but have rarely been studied in that context. What is emerging in studies about the issues noted above are the complex and dynamic interrelationships between climate change, ambient meteorological and micrometeorological conditions, the micrometeorology within individual plants and within their reproductive structures and the knock-on effects on their symbionts (mutualists and herbivores) as ecologically co-dependent partners. In this study we have concentrated on the hitherto unrecognized diversity of heliocaminiform structures and the microgreenhouse effect by which plants may respond to climate change at global to highly localized (including within plant parts) levels.