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
1
Department of Environmental Biology, University of Adelaide, Adelaide, SA 5005, Australia; E-mail:
roger.seymour@adelaide.edu.au
223
0144-8463兾01兾0400-0223$19.50兾0  2001 Plenum Publishing Corporation
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Seymour
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.
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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 evaporation兾condensation. 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).
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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 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.
Temperature Regulation in Thermogenic Flowers
229
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.
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.
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Seymour
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.
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
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).
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Seymour
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
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
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Seymour
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 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.
Temperature Regulation in Thermogenic Flowers
235
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