Essay 11.4
Temperature Regulation by Thermogenic Flowers
Roger S. Seymour, Environmental Biology, University of Adelaide, Australia; Kikukatsu Ito, Cryobiosystem Research Centre, Iwata University, Moroika, Japan
September, 2006
Over 200 years ago the French biologist, Jean-Baptiste de Lamarck, wrote that the blossom of a European arum lily warmed up during the sequence of blooming (de Lamarck 1803–1815). Since then, botanists have recorded significant self-heating in the flowers, inflorescences or cones in several families of plants, including the lotus (Nelumbonaceae), many species of arum lilies (Araceae), and a few species of water lilies (Nymphaeaceae), Dutchman′s pipes (Aristolochiaceae), palms (Arecaceae and Cyclanthaceae), custard apples (Annonaceae), magnolias (Magnoliaceae), Illicium (Illiciaceae), Rafflesia (Rafflesiaceae), winter′s bark (Winteraceae) and cycads (Cycadaceae). These groups are all primitive seed-plants with rather large, fleshy floral structures that are often associated with beetle, bee, or fly pollinators. Heat production is usually thought to enhance the production and dispersal of floral scents that make the plants more attractive, but in some cases it may prevent freezing of the plant or be a reward to insects by keeping them warm in floral chambers where they remain overnight (Meeuse and Raskin 1988; Seymour and Schultze-Motel 1997).
Some species, such as the arum lilies, are so intensely thermogenic that their flowers can increase up to 35°C above the surroundings. For example, in Brazil, the inflorescence of Philodendron selloum is capable of warming to over 40°C at air temperatures close to freezing (Figure 1) (Nagy et al. 1972; Seymour 1999). Skunk cabbage, Symplocarpus foetidus, in North America and Japan, can maintain temperatures above 15°C when the air temperature drops to -15°C, and it often melts the snow around it (Knutson 1974).
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| Figure 1 Thermal image of the inflorescence of Philodendron selloum during thermogenesis (Ito and Seymour 2005). The warm spadix is visible, because the spathe (V-shaped structure) has been cut away. Sterile male florets in the center of the spadix are warmest, but the fertile male florets also produce heat. Female florets at the base of the spadix do not produce significant heat. (Click image to enlarge.) |
Heat production occurs by rapid respiration in the thermogenic cells of the flowers. In most thermogenic species studied so far, the substrate for respiration is starch, often imported in the form of sucrose from other parts of the plant, but in P. selloum, the substrate is lipid that is stored in the florets prior to blooming (Seymour et al. 1984). Analysis of heat production by direct calorimetry and respirometry show that all of the energy in the substrates ends up as heat in P. selloum (Seymour et al. 1983) and in the lotus, Nelumbo nucifera (Lamprecht et al. 1998). Although there is the possibility of some energy going into synthesis of floral structures, this appears to be negligible.
Most of the energy flowing through the respiratory pathways appears to take the alternative (cyanide-insensitive) pathway, branching from the cytochrome pathway at the level of ubiquinone to an alternative oxidase (AOX) in the inner membrane of the mitochondria (Sluse and Jarmuszkiewicz 2002). Because electron transfer through the alternative oxidase is not coupled to proton translocation, two of the three sites of energy conservation are bypassed, and the free energy is released as heat. The AOX pathway seems to be present in all plants at variable capacities, but it is particularly active in thermogenic species (see Web Topic 11.1). The AOX gene is expressed strongly during thermogenesis in carbohydrate-burning arums such as Dracunculus vulgaris (Ito and Seymour 2005). In lipid-burning P. selloum, however, heat production may be associated with uncoupling proteins (UCPs) (Ito and Seymour 2005). These also exist on the inner mitochondrial membrane and permit influx of protons without phosphorylation, the energy ending up as heat (Ito 1999). Interestingly, a similar kind of UCP (the 5 transmembrane-spanning variant UCP1) is used by mammals, particularly hibernating species, which generates heat by burning lipid in brown adipose tissue.
The respiratory rates of some thermogenic flowers are the highest among plants, and in fact, exceed even those of warm-blooded animals. For example, the tissues of Arum maculatum and Helicodiceros muscivorus produce up to about 400 mW g-1 (Lance 1974; Seymour et al. 2003a), while a flying hummingbird produces only 240 mW g-1. At an air temperature of 10°C, a 125 g inflorescence of P. selloum produces about five times the amount of heat of a 125 g rat under the same conditions. Such high rates of heat production demand a good supply of oxygen. In the florets of P. selloum, this is achieved by diffusion through a network of tiny intercellular gas spaces that permeate the tissue to the center. Oxygen demand is so high that the oxygen partial pressure at the center of the floret drops to about one-quarter of atmospheric, but remains just above the critical level where oxygen uptake becomes diffusion-limited (Seymour 2001).
A few species of the most powerfully thermogenic flowers also exhibit temperature regulation, which is the maintenance of a relatively constant temperature in the flower, regardless of external air temperature. This was first demonstrated in P. selloum, but subsequently clearly shown to occur in other arum lilies and also in the lotus, Nelumbo nucifera (Seymour and Schultze-Motel 1998). In these cases, the respiratory rate increases almost linearly as the ambient temperature drops below 30ºC, and the mean temperature of the flower is almost constant (Figure 2). According to simple physics of heat flow, to achieve a stable temperature by the flower, its rate of heat production must be proportional to the temperature difference between it and the air.
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| Figure 2 Rate of oxygen consumption and heat production (top) and temperature of the central receptacle (bottom) in the sacred lotus Nelumbo nucifera, in relation to ambient temperature (Seymour and Schultze-Motel 1998). The dashed line is isothermal, showing that evaporative heat loss predominates at high ambient temperatures, but metabolic heat production prevails at low ambient temperatures. The means were derived from intact flowers in the field, during the thermoregulatory period associated with female receptivity. (Click image to enlarge.) |
The precision of temperature regulation is exceptional in the lotus. Heat production occurs in the receptacle of the flower, and its mean temperature is 30°C when ambient temperature is 10°C, rising to 36°C when the effective ambient temperature in the sun rises to 45°C (see Figure 2). Thus flower temperature varies only 6°C while ambient temperature varies 35°C. At low ambient temperatures during the night, heat production by the flower rises to about 1 W, but it decreases to about 0.3 W during the day. Although still respiring on hot days, the flower temperature drops as much as 10°C below effective ambient temperature by evaporative cooling. The flower clearly responds to ambient temperature, not light level (Seymour et al. 1998).
It is apparent that the flowers cannot detect ambient temperature directly but only respond to changes in the temperature of their own cells. Close examination of the data reveals that there is a small decrease in flower temperature that occurs with falling ambient temperature (see Figure 2). Therefore, it is clear that respiration in these species is negatively related to tissue temperature, opposite to the expected positive relationship between temperature and rates of biochemical reactions.
The relationship between ambient temperature, tissue temperature, and respiration rate has been demonstrated in the field for S. foetidus (Figure 3). At ambient temperatures between about 5–25ºC, small (2 g) spadices of these plants are able to thermoregulate in a range between 18–25°C. Within this range, decreasing ambient temperature causes spadix temperature to decrease and heat production to increase. The maximum rate of heat production that the florets can produce occurs at about 18°C, which is the watershed for thermoregulation. If temperature drops below this point, the inflorescences can no longer produce enough heat to remain warm, so they must cool to about ambient. Thus, they abruptly "switch off their thermostats" at low ambient temperatures, but they can switch them back on if ambient temperatures rise. The switching point apparently depends on spadix size. Larger spadices (4.5 g) can remain warm at air temperatures down to -15°C (Knutson 1974). Part of the variation in spadix temperature also results from thermal lags in plants measured in changing conditions in the field (Knutson 1974; Seymour and Blaylock 1999). In a temperature-controlled enclosure, set at constant temperatures between -10ºC to 27ºC, spadix temperature remains in the narrow range between 22.7ºC and 26.2ºC (Seymour 2004).
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| Figure 3 Relationship of oxygen consumption rate and inflorescence (spadix) temperature in Eastern skunk cabbage Symplocarpus foetidus measured in the field in Ontario, Canada (Seymour and Blaylock 1999). The points were gathered at 24-minute intervals from a single plant over a period of 5 days. Peak respiration occurs at a spadix temperature of about 18°C, which occurs at an ambient temperature of about 3°C. Above this level, the cluster of points at the upper right demonstrates the inverse relationship between respiration and spadix temperature. When ambient temperature drops below about 3°C, however, heat production cannot be sustained, and spadix temperature drops quickly to just above ambient, resulting in the cluster of points at the lower left. (Click image to enlarge.) |
The physiological thermoregulatory control mechanism is not known. It is certain, however, that it is unlike the mechanism in birds and mammals that relies on a complex nervous interaction between temperature receptors, central nervous system processing, and finally, control of organs that affect rates of heat production and loss. In plants, the regulation must occur at a strictly biochemical level. Inhibition of enzyme activity by high temperature is common. Warming of the plant tissues could conceivably cause gradual inhibition of heat-producing biochemical reactions as enzymes change structure or position on fluid membranes. The problems with this idea are that the inhibition is completely reversible, it sometimes occurs at relatively low temperatures (e.g., 18–25°C in skunk cabbage), and it occurs relatively slowly. For example, it takes about 1–2 hours for the lotus to decrease respiration when exposed to warm conditions and about the same time for an increase in response to cold (Seymour and Schultze-Motel 1998). These lags suggest that temperature regulation occurs by synthesis or activation of some regulatory molecule, possibly AOX and UCP.
Temperature regulation is an adaptation shared by homeothermic (warm-blooded) birds and mammals and many groups of flying insects. High and stable body temperatures permit them to be active in cold environments. Compared to thermally compliant poikilotherms (cold-blooded animals), animal homeotherms are able to find more food, better compete for territory and mates, and reproduce faster—all evolutionarily advantageous in many circumstances. So, homeothermy in immobile flowers is at first difficult to explain. Temperature regulation is not a requirement to enhance the vaporization of scents; unregulated high temperatures would suffice, as they do in Dracunculus vulgaris (Seymour and Schultze-Motel 1999). However, we now have the first evidence that thermoregulation in the flowers is a service offered as a reward to insect visitors (Seymour et al. 2003b). Thermoregulatory flowers are often pollinated by large flying insects, chiefly beetles, which remain within the flower for about 24 hours. For example, large scarab beetles congregate in the evening inside the floral chamber of Philodendron solimoesense in lowlands French Guiana, and they are active throughout the night, consuming floral parts and mating avidly (Figure 4). These activities apparently require high body temperatures, because the beetles raise their temperature by a kind of "shivering" that involves heat-generating contractions of their flight muscles. However, the energy cost of this activity inside the floral chamber is some 2–4 times less than it would be outside, despite a chamber temperature only 4ºC warmer than the outside air. The energy savings of beetles could be much greater inside Philodendron in cooler air at higher altitudes. While many nonthermoregulatory flowers offer energy in the form of nectar, starch, or pollen to their insect visitors, thermoregulatory flowers can offer energy directly as heat. In return, the beetles transfer pollen each day from one flower to the next.
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| Figure 4 Mating scarab beetles (Cyclocephala colasi) on the sterile male florets of Philodendron solimoesense in French Guiana (Seymour et al. 2003b). The beetles have gnawed some of the florets (lower left). Beginning in the evening, these activities continue throughout the night. The beetles rest in the floral chamber the next day and depart for a new, warm inflorescence the following evening. (Click image to enlarge.) |
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