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Biophysics and Physiology of Temperature Regulation in Thermogenic Flowers

Article in Bioscience Reports · May 2001
DOI: 10.1023/A:1013608627084 · Source: PubMed

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Bioscience Reports, Vol. 21, No. 2, April 2001 ( 2001)

MINI REVIEW

Biophysics and Physiology of Temperature Regulation in

Thermogenic Flowers
Roger S. Seymour1
Receiûed October 26, 2000

The flowers or inflorescences of certain primitive seed plants are able to regulate their
temperature during blooming by modulating the rate of heat production to remain much warmer
than the surroundings. A large drop in ambient temperature causes a smaller drop in flower
temperature which causes an increase in the rate of heat production by futile involvement of the
cytochrome and alternative oxidase respiratory pathways. The result is that the rate of heat
production is inversely related to ambient temperature and flower temperature remains high and
relatively independent of ambient temperature. While the biophysics of thermal balance in the
whole flowers is better understood, the regulation of the biochemical heat-generating pathways
is not known.

KEY WORDS: Thermogenic flowers; respiration; cytochrome oxidase; alternative oxidase;

plant mitochondria; thermal inhibition; plant biochemistry.

INTRODUCTION
For over 200 years, botanists have known that the flowers of some plants become warm
during the sequence of blooming. Some species, such as Philodendron selloum (Nagy et
al., 1972) and Symplocarpus foetidus (Knutson, 1974), are so intensely thermogenic that
their flowers can heat up to 35°C above their surroundings. Significant self-heating
occurs in the flowers, inflorescences or cones of some species in several families of
primitive seed-plants, namely the aroids, or arum lilies (Araceae) (Meeuse and Raskin,
1988), lotus (Nelumbonaceae) (Miyake, 1898; Schneider and Buchanan 1980) water
lilies (Nymphaeaceae) (Prance and Arias, 1975), Dutchman’s pipes (Aristolochiaceae)
(Raskin et al., 1987), palms (Arecaceae and Cyclanthaceae) (Schroeder, 1978;
Gottsberger, 1990; Listabarth, 1996) custard apples (Annonaceae) (Gottsberger, 1990),
magnolias (Magnoliales) (Thien et al., 1999; Schultze-Motel, unpubl.) and cycads
(Cycadaceae) (Skubatz et al., 1993). Explanations for heat production include
enhancement of scent production (Meeuse and Raskin, 1988), protection from freezing
(Knutson, 1979), and a thermal reward to insect pollen vectors (Seymour and Schultze-
Motel, 1997).
Many thermogenic flowers produce heat at variable and apparently uncontrolled rates, and
their temperatures vary widely during the flowering sequence. A
 224 Seymour

1
Department of Environmental Biology, University of Adelaide, Adelaide, SA 5005, Australia; E-mail:
roger.seymour@adelaide.edu.au
223
0144-8463010400-0223$19.500  2001 Plenum Publishing Corporation
few species, however, adjust the rate of heating in relation to ambient temperature such
that the flower temperature remains somewhat independent of ambient temperature. This
phenomenon is known as physiological temperature regulation. Temperature regulation
was first discovered in the arum lily P. selloum (Nagy et al., 1972) and subsequently in
eastern skunk cabbage S. foetidus (Knutson, 1974), the sacred lotus Nelumbo nucifera
(Seymour and Schultze-Motel, 1996) and the dragon lily Dracunculus ûulgaris (Seymour
and Schultze-Motel, 1999). It may also occur in the arum lilies Sauromatum guttatum
and Xanthosoma robustum (Meeuse and Raskin, 1988). Similar patterns of flower
temperature and rate of heat production in response to ambient temperature occurs in all
of these species; as ambient temperature decreases, the difference between flower and
ambient temperature increases and the rate of oxygen consumption increases (Fig. 1).
Temperature regulation is usually attributed to endothermic animals, such as
mammals and birds, although it does occur in many flying insects. In the animals,
regulation is mediated by a complex interaction between thermal receptors in the body,
integrative and regulative centers in the brain, and effector organs that alter the animal’s
insulation, augment heat production or invoke evaporative heat loss. It is fascinating that
temperature regulation can be as effective in some flowers that lack these mechanisms.
Regulation in flowers occurs mainly by modulating the rate of heat production, and the
control apparently occurs at the cellular level. This review explores the phenomenon in
thermoregulating flowers, presents a biophysical model for heat balance, compares the
precision of regulation, and proposes potential biochemical temperature control
mechanisms.

REQUIREMENTS OF A THERMOREGULATORY SYSTEM

A thermoregulatory system requires a mechanism that controls the rates of heat flux.
As ambient temperature declines, the rate of heat loss increases because of a rising
temperature difference between the flower and the surroundings. This causes flower
temperature to decrease somewhat, which must ultimately be the stimulus for increasing
heat production. In most biochemical systems, however, a decrease in temperature results
in a decrease in metabolic rate. It is therefore apparent that the opposite must occur in
thermoregulating flowers: the rate of heat production must increase as flower temperature
decreases. The first evidence of inverse temperature dependence appeared in
measurements of spadix temperature and oxygen consumption in P. selloum (Nagy et al.,
1972). When whole spadices were cut and incubated at selected ambient temperatures
between 4–39°C in the laboratory, maximum spadix temperature varied between 39–
44°C and oxygen consumption decreased at higher floret temperatures (Fig. 2).
Thermal inhibition of respiration because of denaturation of enzyme systems is not
unusual at high tissue temperatures in many organisms, but in the case of
thermoregulating flowers, the inhibition is reversible and enzyme denaturation seems
unlikely. Reversibility can be shown in P. selloum by cutting the sterile male florets from
the spadix and measuring oxygen consumption directly at test floret temperatures
between 39–44°C (Seymour et al., 1983). Oxygen consumption is high at 39°C,
decreases at 44°C and recovers virtually completely when floret temperature is
Temperature Regulation in Thermogenic Flowers 225

Fig. 1. Effect of ambient temperature on mean rates of oxygen consumption and flower temperature in
the sacred lotus Nelumbo nucifera during the 2–4 day thermoregulatory period in an outdoor pond
(Seymour and Schultze-Motel, 1998). Note that the rate of oxygen consumption, indicative of the rate
of heat production, increases linearly as ambient temperature decreases. Meanwhile flower temperature
remains between about 30 and 36°C. Evaporative cooling is sufficient to depress flower temperature
several degrees below at high ambient temperatures in the sun. The dashed line is isothermal.

returned to 39°C. Significantly, the responses to temperature change are not immediate;
recovery time is 20 min after exposure to 44°C, and longer at higher temperatures. The
measurements from P. selloum suffer from the facts that cut spadices or florets are
triggered into a single, intense episode of thermogenesis that lasts only 1– 2 hr and the
rate of heat production never stabilizes. Therefore it is not possible to examine the effects
of floret temperature on heat production throughout a broad range of temperature or over
longer periods of time.
226 Seymour

Fig. 2. Effect of floret temperature on rate of oxygen consumption of

isolated sterile male florets of Philodendron selloum during maximal
thermogenesis (Seymour et al., 1983). Notice the steep, inverse decrease
in respiration at temperatures above 37°C. Means and 95% confidence
intervals are given.

In contrast to the short-lived thermogenesis in cut P. selloum inflorescences, those

of another arum lily, S. foetidus (eastern skunk cabbage), remain thermogenic for a week
or more, and under widely fluctuating ambient temperatures in the field (Knutson, 1974).
Recent work in Canada shows the thermal and respiratory responses of the inflorescence
to ambient temperature changes between −12 and 24°C (Seymour and Blaylock, 1999).
At ambient temperatures between about 3– 24°C, spadix temperature varies between 16–
26°C by increasing heat production as ambient temperature decreases. The inverse
relationship between the respiratory rate and spadix temperature above 16°C is clearly
shown in measurements of oxygen consumption over several days in the field under
naturally fluctuating ambient temperature (Fig. 3).

SWITCHING BETWEEN THERMOREGULATORY AND NON-

THERMOREGULATORY STATES
Inflorescences of S. foetidus thermoregulate at ambient temperatures above about
3°C when spadix temperature is above 16°C (Fig. 3). When ambient temperature drops
below about 3°C, however, the spadix temperature decreases below 16°C and respiration
begins to decline. With a lower heating rate, spadix temperature falls lower, further
decreasing respiration. The result is that spadix temperature quickly declines to
approximately 0°C. Upon rising ambient temperature, the spadix can
Temperature Regulation in Thermogenic Flowers 227

Fig. 3. Rate of oxygen consumption in Symplocarpus foetidus

inflorescences in relation to spadix temperature. The data were taken at
24min intervals during a 5-day period when the spadix switched between
warm and cool states (Seymour and Blaylock, 1999). Spadix switching
temperature is about 16°C.

resume higher levels of heat production, switching to the regulated state above 16°C. The
result is that the inflorescence switches between the warm and cool states if the ambient
temperature varies above and below approximately 3°C. The rate of heat production is
maximal at a spadix temperature of 16°C, and it decreases quickly at lower temperatures;
therefore this temperature is known as the ‘‘switching temperature.’’ The distribution of
data for the relationship between respiratory rate and spadix temperature of S. foetidus
(Fig. 3) shows the switching temperature and reveals that the inflorescence tends to be
either warmer than 16°C or colder than 6°C, with few intermediate points. This bimodal
distribution is also seen in randomly sampled spot measurements of spadix temperature
in the field. In one survey when ambient temperatures were close to freezing, one group
of plants averaged 3.8°C while the other group averaged 17.0°C (Seymour and Blaylock,
1999).

BIOPHYSICAL MODEL OF THERMOREGULATION AND

SWITCHING TEMPERATURE
The temperature of an object depends on factors that affect the rates of heat flux to
or from it. In biological systems, heat is produced by catabolic biochemical reactions.
Heat may be gained or lost by radiation, convection, conduction and the latent heat of
evaporationcondensation. Any object will passively reach a certain temperature when
these avenues are balanced. If the object is completely passive, it will reach a
temperature determined by its thermal environment, that is, a temperature determined by
the integrated effects of radiation, convection, conduction, evaporation and metabolism.
These factors interact in a complex way that can be approximated or modeled with
biophysical principles (Nobel, 1999).
The bimodal distribution of S. foetidus spadix temperatures results from biophysical
relationships between rates of heat production, rates of heat loss, spadix temperature and
ambient temperature that reveal stable temperature equilibria at either high or low
 228 Seymour
temperatures. These equilibria are shown by intersections between curves for heat
production and heat loss derived from field data (Fig. 4). The intersections are stable,
because the slope of the relationship for heat production is less than that for heat loss.
Therefore spadix temperatures below the intersection cause heat production to exceed
heat loss, while temperatures above it cause heat loss to exceed production. In both cases,
the imbalance is resolved when spadix temperature is drawn toward the intersection. The
inverse relationship between spadix temperature and heat production above the switching
point of about 16°C defines the region of warm temperature regulation in S. foetidus (Fig.
3).
The balance between heat production and heat loss is affected not only by ambient
temperature, but also by the characteristics of the inflorescence. Larger spadices are
better able to produce heat and retain it because of the ratio of surface (which partly
determines the rate of heat loss) and volume (which partly determines the rate of heat
production). This effect is apparent in studies of S. foetidus involving different sized
inflorescences. Spadix size in one population was about 2 g and they were unable to
remain warm at ambient temperatures below about 3°C (Seymour and Blaylock, 1999),
while those in another population averaged 4.5 g and remained warm at ambient
temperatures down to −14°C (Knutson, 1974). In these cases, the

Fig. 4. Biophysical model of heat production and heat loss in Symplocarpus

foetidus, based on oxygen consumption and thermal conductance data from
inflorescences in the field (Seymour and Blaylock, 1999). The sigmoid
polynomial function for heat production is superimposed on curves for heat
loss in relation to spadix temperature. The heat loss curves shift position,
depending on environmental temperature. Stable spadix temperatures occur
at the intersections of the curves and their positions depend on
environmental temperature.
switching temperatures of the spadices remained near 16°C, but higher rates of heat
production in the larger spadices permitted them to remain above this temperature at
lower ambient temperatures. Most large spadices (>100 g) of P. selloum can warm to
about 40°C at air temperatures near freezing, but smaller spadices fail to warm at 4°C
(Nagy et al., 1972). In this case, switching temperature of the spadix is about 37°C.
Temperature Regulation in Thermogenic Flowers 229
PRECISION OF THERMOREGULATION
The temperatures achieved by thermoregulating flowers depend somewhat on
ambient temperatures. With increasing ambient temperature, flower temperature rises.
The slope of this linear relationship is a measure of the precision (sometimes called
‘‘gain’’) of temperature regulation. Perfect independence of flower temperature from
ambient temperature would produce a slope of zero, and complete dependence yields a
slope of 1.0. Perfect independence is not possible, because the changes in rate of heat
production ultimately depend on flower temperature which must drop in order to cause
an increase in heating rate. Comparison of the four species of thermoregulating plants
reveals significant differences in precision of regulated temperature (Fig. 5). The most
precise thermoregulating species are the lotus N. nucifera, with a slope of 0.17 (Seymour
and Schultze-Motel, 1998) and P. selloum with a slope of 0.18 during the peak heating
phase (Nagy et al., 1972). In another study of P. selloum, regulation was precise (0.19) in
the peak phase of warming on the first evening of flowering, but was less precise (0.52)
in the plateau phase that occurs

Fig. 5. Relationships between temperatures of flowers and the environment in

four species of thermoregulatory plants. The slopes of the lines indicate the
precision of thermoregulation. A horizontal line (slopeG0) would indicate
ideally perfect temperature regulation while the line of equal temperature
(slopeG1) indicates no regulation. Sources of data are provided in the text.
during the next 12 hr (Seymour, 1999). Less precise regulation occurs in S. foetidus with
slopes of 0.29 in large inflorescences (Knutson, 1974) and 0.51 in small ones (Seymour
and Blaylock 1999). Similarly, the slope is 0.59 in D. ûulgaris (Seymour and Schultze-
Motel, 1999). Interestingly, it is apparent from the available data that flowers that
regulate at higher temperatures are more precise (Fig. 5). While it might be thought that
greater precision is possible in flowers that are better insulated or of larger size, the
inflorescences of P. selloum show greater precision during the first episode of peak heat
than in the longer plateau stage (Fig. 5). The precision of thermoregulation should reflect
the slope of the relationship between rate of respiration and flower temperature above the
switching temperature. The steeper the inhibition of respiration at high temperatures, the
greater the precision of thermoregulation.
230 Seymour
REGULATED VS. UNREGULATED HEAT PRODUCTION
High variability in precision of temperature regulation in the four species so far
studied in detail reflects a far greater variability in intensity and precision of all
thermogenic flowers. It is clear that heat production is not regulated in the cones of
cycads, the inflorescences of several species of arum lily, and the flowers of water lilies
and magnolias (Seymour and Schultze-Motel, unpubl.). In these cases, the role of heat
production may be an enhancement of scent production, as usually rationalized, or a by-
product of tissue growth.
The inflorescence of D. ûulgaris, however, reveals that there can be regulating and
non-regulating tissues in the same plant (Seymour and Schultze-Motel, 1999). In this
species, the spadix is divided into two parts, the spadix proper and the appendix. The
spadix is surrounded by its male and female florets in a floral chamber that is enclosed in
a bulb derived from the lower part of the spathe (Fig. 6). The large appendix is an
extension of the spadix that protrudes out of the floral chamber and extends in the air
above the open part of the spathe (Fig. 6). This inflorescence shows a pattern of warming
that follows, in a meaningful way, the sequential periods of (1) attraction of flying
insects, (2) receptivity of the female florets (3) entrapment of insects, (4) release of
pollen from male florets, and (5) release of insects. The florets in the floral chamber
warm weakly on the first night of spathe opening, but this seems to have no significance.
This minor heating decreases the next day and is replaced by a powerful production of
heat by the appendix that peaks in the middle of the day and subsides by sunset. The
appendix produces a powerful scent of rotten meat and attracts flying beetles and flies.
The beetles land on the liver-colored spathe and fall into the floral chamber where they
pollinate the receptive female florets. Slippery walls of the floral chamber trap them for
up to 22 hr, including the second night. During this night, from sunset to the following
morning, the floral chamber again warms, but this time it is more powerful and
thermoregulatory. Warming wanes the next morning when pollen is shed on the trapped
beetles which are then released from the floral chamber. During the period of insect
attraction, the appendix produces a great deal of heat and scent, but it does not regulate
its temperature, as shown by the direct relationship between oxygen consumption and
ambient temperature (Fig. 6). On the other hand, during the period of insect entrapment
on the
Temperature Regulation in Thermogenic Flowers 231

Fig. 6. Respiration rate and temperatures in the inflorescence of

Dracunculus ûulgaris during its triphasic series of thermogenesis: floral
chamber (1st night), appendix (day), floral chamber (2nd night). Oxygen
consumption rate indicates rate of heat production in the appendix and floral
chamber. Similarity of appendix and ambient temperature and decreasing
oxygen consumption at lower ambient temperature show that the appendix
produces significant heat but does not thermoregulate or warm appreciably.
Elevation of floral chamber temperature and an inverse relationship between
oxygen consumption and ambient temperature demonstrate thermoregulation
by the florets, especially during the second night when insects are trapped in
the chamber. Means and 95% confidence intervals are given for 2°C
temperature intervals; the dashed line is isothermal. The data are from
Seymour and Schultz-Motel (Seymour and Schultze-Motel, 1999).
second night, the floral chamber is regulated at about 18°C and the heat production rate
of the florets is inversely related to ambient temperature (Fig. 6). It is clear that
temperature regulation is not associated with scent production, but rather with insect
entrapment. D. ûulgaris therefore demonstrates that thermoregulation is specific to
232 Seymour
certain parts of the plant and is not always associated with all thermogenic tissues. The
species also shows that measurements of floral temperatures are poor indications of the
rate of heat production. In this case, most of the heat generated by the inflorescence
comes from the appendix and relatively little from the spadix. Almost all of the heat from
the appendix is lost by evaporation, so appendix temperature does not rise (Fig. 6).

BIOCHEMICAL BASIS FOR TEMPERATURE REGULATION

The pattern of temperature regulation is the same in the four species that have been
well studied; there is a small change in flower temperature over a broad range of ambient
temperature (Fig. 5). It is apparent that the rate of heat production depends inversely on
flower temperature within its thermoregulatory range by a reversible thermal inactivation
of respiration at higher flower temperatures.
Temperature regulation in these flowers occurs in the cells and may be functionally
linked to the alternative (cyanide-insensitive) respiratory pathway, branching from the
cytochrome pathway at the level of ubiquinone to an alternative oxidase (AOX) in the
inner membranes of the mitochondria (Elthon and McIntosh, 1986, 1987; Elthon et al.,
1989). Thus the pathway bypasses the energy conserving sites of the cytochrome-based
pathway, no proton electrochemical gradient is generated across the membrane, and the
chemical energy of the respiratory substrate is dissipated as heat. The alternative pathway
seems to be present in all plants, although at variable levels (Siedow and Berthold, 1986),
but it is particularly active in Nelumbo (Skubatz et al., 1990) and in several arum lilies
(Meeuse and Raskin, 1988). In Arum maculatum, for example, almost all respiratory
oxygen consumption is ûia the AOX (Moore and Siedow, 1991). Measurements of heat
production and oxygen consumption in the sterile male florets of P. selloum show that all
energy derived from respiration is lost as heat, and there is no apparent energy conserved
in synthesis (Seymour et al., 1983).
The alternative pathway is known to be thermally labile. For example, respiration of
isolated arum lily mitochondria decreases steeply at temperatures above 40°C (Chauveau
et al., 1978), which may account for the reversible thermal inhibition of respiration that is
responsible for temperature regulation. Thermal inhibition need not be exclusively a high
temperature phenomenon, moreover. Inhibition apparently occurs at temperatures above
about 16°C in skunk cabbage S. foetidus (Seymour and Blaylock, 1999) and 18°C in the
dragon lily D. ûulgaris (Seymour and Schultze-Motel, 1999).
A common characteristic of all thermoregulating flowers that provides a clue to the
regulatory mechanism is a pronounced latency (time-lag) between temperature change
and the regulatory adjustment. For example, it requires about 2–3 hr for N. nucifera to
increase its heat production in response to decreasing ambient temperature at the end of
the day, and a similar time to decrease heat production in the
Temperature Regulation in Thermogenic Flowers 233

Fig. 7. Relationship between respiratory rate and temperature of the heat-

producing receptacle in Nelumbo nucifera flowers in an outdoor pond
(Seymour and Schultze-Motel 1998). Data from 18 flowers have been
averaged at hourly intervals throughout the 24-hr cycle as indicated by times
adjacent to some symbols. Means and 95% confidence intervals are
presented.

morning (Fig. 7). When water-jacketed Nelumbo are artificially exposed to sudden
ambient temperature changes, they show a two-phase reponse (Seymour et al., 1998).
Cold air results in immediate cooling of the flower and a sharp drop in oxygen
consumption (a mass-action effect), followed by a slow regulatory rise in oxygen
consumption and rewarming; warm air produces the opposite effects. A similar latency
appears in P. selloum (Seymour et al., 1983) and S. foetidus (Knutson, 1979) following
temperature change. Thermal inhibition of individual enzymes, or changes in enzyme
activity due to alterations in membrane structure and fluidity are likely to occur
immediately with temperature change (Steponkus, 1981). On the other hand, the
response latency of 2–3 hr may indicate the involvement of intermediate metabolic
regulators that act on rate-limiting enzymes, possibly the AOX, involved in heat
production. Such response latency may be associated with slow changes in the
concentrations of regulatory substances. It is known, for example, that organic acids such
as pyruvic acid activate the alternative pathway in mitochondria of several plant species,
including thermogenic arum lilies (Day et al., 1995). Cold exposure for 8 hr is also
known to activate respiration in a variety of chill-sensitive plant species (Moynihan et
al., 1995). Alternatively, it is possible that regulation occurs by protein synthesis.
Vanlerberghe and McIntosh (1992) reported an increase of AOX activity in tobacco cells
after transfer from 30°C to 18°C due to de noûo synthesis of the protein.
Recent investigations on the biochemical control of thermoregulatory responses
have been carried out with the thermogenic receptacle tissue of N. nucifera (Beardall,
Seymour and Baldwin, unpubl.). The respiratory capacities of the alternative and
cytochrome pathways were compared in tissues obtained at two times of day when
respiration was either high or low. In the cool morning, flower temperature was about
30°C and thermogenesis was high; in the warm afternoon, the flower was about 36°C
and thermogenesis was low (Fig. 7). Plugs of tissue were incubated at 30°C or 36°C in
the presence of either cyanide (to block the cytochrome pathway) or propyl gallate (to
 234 Seymour
block the alternative pathway) or both. Rates of oxygen consumption during these
treatments indicated the relative capacities of the two pathways, but not the actual
activities in untreated tissue. Nevertheless, in the morning, the capacity of the alternative
pathway was high and it was markedly inhibited when exposed to 36°C. In the afternoon,
the alternative pathway was lower at 30°C and less sensitive to exposure to 36°C. The
capacity of the alternative pathway was very low in non-thermogenic buds, increased
threefold in thermoregulatory stages and decreased again in older flowers that have no
thermoregulatory ability. By contrast, the capacity of the cytochrome pathway appeared
to decrease during the thermoregulatory phase. These results suggest that temperature
regulation involves the alternative pathway to a significant extent, but further work is
required to measure activities of both pathways under natural conditions and to
determine the mechanism for regulation of activity.

CONCLUSION
There is no doubt that the phenomenon of temperature regulation in flowers seems
bizarre and few people are carrying out research in the area. Only my laboratory is
apparently actively seeking a biochemical explanation for it. Part of the reason may be
that so few thermoregulating plants have been discovered so far, and they are considered
to be mere curiosities. However, the phenomenon may have been much more common
during the early history of seed plants than it is today. The simultaneous radiations of
seed plants and beetles in the late Mesozoic era suggest that thermoregulatory flowers
may have commonly provided warm refuges for endothermic, flying beetles (Seymour
and Schultze-Motel, 1997). The direct application of heat and the stability of temperature
may have been an energetic reward that may have been as important to pollination
biology then as the nectar and pollen rewards are today. Aside from the ecological and
evolutionary implications of studies on thermoregulatory flowers, the phenomenon may
have wider application for plant (and even animal) respiratory control systems. For
example, inhibition of heat production at high tissue temperatures may influence
respiration of plant tissues warmed by the sun, or it may be associated with the limitation
of body temperature in humans during fever.

ACKNOWLEDGMENTS
I appreciate the invitation by Professor Leopoldo de Meis to write this review and
Drs John Beardall, John Baldwin, and Paul Schultze-Motel for unpublished material.
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