Heat-producing flowers
Roger S. Seymour and Paul Schultze-Motel
The flowers of some plants produce enough heat to raise their temperatures as much as 35°C above air
temperature. Three species have been shown to regulate flower temperature within a narrow range by an
unknown physiological
mechanism that increases the rate of heat production as air temperature
decreases. Thermogenic plants occur only in ancient families of seed plants, and have apparently
evolved in association with beetle pollinators. Because many beetles require high body temperatures for
activity, the warm environment inside thermoregulating flowers may be an energetic reward during their
visits.
Evolution of flowering plants has produced
an astounding
diversity of reproductive
‘strategies’ that promote cross-pollination
[l]. Many flowers attract animal vectors,
principally insects and birds, and reward
them with energy. The attractants are generally conspicuous blossoms, often associated
with chemical scents, and the rewards are
usually nectar, starch and pollen. Some
insect-pollinated
flowers attract their visitors by resembling something they are not,
for example another insect to mate with, or
a dead animal to lay eggs in, and a reward
may not be forthcoming. One of the more
unusual tactics occurs in flowers that raise
their temperatures by producing their own
heat. Although heat production is usually
considered by botanists to augment scent
vaporization
to make the flower more
attractive [2], in some cases it may also be a
direct energy reward for insect visitors.
Evidence for the latter idea comes from the
discovery that some flowers maintain a
high, nearly constant internal temperature in
the face of large fluctuations in environmental temperature-the
flowers physiologically thermoregulate - rather like ‘warmblooded’ animals. This article considers
these heat-producing
plants, and concentrates on the role of thermoregulation in the
biology of pollination.
All flowers contain metabolic biochemical activity, the by-product of which is heat;
thus they are all technically ‘thermogenic’.
In most flowers, however, reactions occur
slowly, or heat escapes quickly, and no
appreciable
temperature
elevation takes
place. The plants that botanists recognize as
Roger S. Seymour,
BA, Ph.D.
Is Associate Professor of Zoology at the University
of Adelaide. His usual research involves respiration
and cardiovascular physiology of animals.
Paul Schultze-Motel,
Ph.D.
Is Postdoctoral
Research
Associate
at the
University of Adelaide. His doctoral research concerned temperature regulation in insects.
thermogenic
are those that produce an
unusually large amount of heat, for the
sake of producing it, not as a by-product of
other metabolic
activity.
Accordingly,
thermogenic
flowers are able to raise
their temperature
significantly.
By this
definition, thermogenic flowers and cones
are known to occur in several plant
families
including
Araceae
(aroids or
arum lilies), Aristolochiaceae
(Dutchman’s
pipes),
Nymphaeaceae
(water
lilies),
Nelumbonaceae (true lotuses), Annonaceae
(custard
apples),
Arecaceae
(palms),
Cyclanthaceae
(Panama hat palms), and
Cycadaceae (cycads) [1,3].
A unifying characteristic of thermogenic
flowers is that they are generally large,
because
small
flowers
with
high
surface:volume ratios are unable to retain
enough heat to raise flower temperature
noticeably. Another characteristic of thermogenie flowers is that they are protogynous,
that is, the female parts of the flower mature
first and pollination takes place before the
male parts release pollen. Thus insects that
are attracted to the flower bring in pollen
from other plants and accomplish crossfertilization. They may be physically trapped
by the flower, or encouraged to remain in it
by rewards of food or shelter, until the
female parts become non-receptive and the
male parts release pollen. Then they are
encouraged to leave to carry pollen to other
plants.
Heating enhances attraction
The major episode of heat production in
these plants usually corresponds
to the
period when the female flower parts are
most receptive to pollination and when the
flower’s scent is strongest. Thermogenic
flowers produce aromas that range from
sweet perfumes to nauseating
stenches.
Many species produce indoles and scatoles
that mimic the pungent aroma of decaying
flesh or dung. Carrion beetles and flies
attracted to the plant to feed and lay eggs
may be trapped inside the inflorescence. For
example, the dragon lily, Dracunculus vul-
Copyright 0 1997 Elsevier Scbence Ltd. All right reserved. 0160-9327/97/$17.00.
PII: SO160-9327(97)0104
guris, from the Mediterranean region, produces half-metre inflorescences consisting
of a dark purple spadix encased in a leathery
spathe (Figure l(a)). When the spathe opens
in the morning to reveal its dark purple
inside surface, which resembles liver, the
spadix begins to produce heat and a horrific
odour reminiscent of a dead cat. Pollenbearing insects, chiefly carrion beetles and
flies, find this irresistible and fly in to the
landing area provided by the spathe. Some
fall into the bottom of the chamber and
provide pollen to receptive female florets.
Having performed
their duty, they are
unable to escape because the slippery walls
do not provide a foothold. As heat production subsides the next day, the male florets
shower the insects with pollen, the inner
surface of the floral chamber changes to
provide traction, and they climb out.
Another well-studied
example is the
Amazon water lily, Victoria amuzonica,
which combines heat production with a
change in petal colour to control the behaviour of beetle pollinators during a two-day
sequence (Figure l(b)) [4]. Beautiful white
petals of these 20 cm flowers open in the
evening of the first day. At this time flower
temperature
rises to about 10°C above
ambient air and a strong fruity odour is produced. The display and scent immediately
attract numerous 1.0-2.5 cm-long scarab
beetles (genus Cyclocephrrla) that fly to the
petals and immediately crowd into the floral
chamber. The upper margin of the chamber
is lined with starchy tissue which the beetles
eat. Later, at night, the petals gradually
close around the gluttonous insects and trap
them inside for the next day. By late afternoon, the closed petals have turned from
white to dark purple. Then, in the evening,
the petals reopen and allow the beetles to
crawl out through the stamens which dust
them with pollen. The insects are not
attracted to this second-day flower because
it is no longer strongly scented, white or
rich with food. Instead, they fly to first-day
flowers, cross-pollinate them, and repeat the
cycle.
Endeavour
Vol. 21(3) 1997
125
The aquatic lotus, Nelumbo nucifera, is
widely distributed through temperate and
tropical regions of the Old and New Worlds.
The lotus flower blooms in a protogynous
sequence; on the first day the flower is
receptive to pollination, as evidenced by
sticky stigmas, and pollen is released on the
second day [5]. First-day flowers open their
petals only slightly - enough to allow entry
to the floral chamber, but not enough to permit access to the stamens at the side of the
receptacle (Figure l(c)). Insects entering the
flower at this time pollinate the stigmas.
The petals close in the afternoon and reopen
widely the next morning, revealing numerous stamens bearing copious pollen on
which insects can feed before leaving for
another flower.
During this sequence, the flower maintains remarkable temperature
stability flower temperature
stays between about
30-36°C while ambient temperature varies
between 10-45” C (Figure 2) [6,7]. The
thermoregulatory
period coincides
with
receptivity of the female parts, beginning
before the petals open and ending when
they open widely. Temperature stability is
achieved by increasing the rate of heat production almost in proportion to the temperature difference between the flower and its
surroundings.
Thus
heat
production
increases progressively as the ambient temperature declines (Figure 3). At high ambient temperatures, heat production is low,
and flower temperature can drop below the
ambient by evaporative cooling.
How does the lotus regulate its
temperature?
Figure 1 Examples of thermogenic flowers in the period of female receptivity. All flowers
have been sectioned to reveal the inner parts. (a) Dracuncu/us vu/garis shows the
odoriferous spadix and dark crimson spathe above. In the floral chamber below, a dark
band of male florets lies on the spadix above the lighter female florets. (b) Victoria
amazonica shows its floral chamber above ovaries embedded in pithy white tissue at the
base. The chamber is ringed above by a row of fleshy, tooth-like protuberances that provide
food for beetles. Upon release, the beetles must crawl through the yellow stamens which
cover them with pollen. (c) Nelumbo nucifera shows its floral chamber under a dome of pink
petals. Female stigmas dot the top of the flat-topped carpellary receptacle, which presses
tightly against the stamina1 appendages on the tips of the stamens (rear), preventing access
to the pollen until the petals open fully. In front, the loss of petals has allowed the stamens
to hang free, as occurs naturally when the petals open fully. (d) Philodendron selloum
shows the central spadix surrounded by the cut spathe. Three floret types are visible on the
spadix: fertile males at the top, heat-producing sterile males in the middle, and females at
the bottom, next to the floral chamber.
Temperature regulation
Measurements
of temperatures
in thermogenie plants have been made for over a century, but most have been opportunistic.
There are few studies that document the
entire course of flowering with continuous
temperature data. Those that do usually
126
Endeavour Vol. 21(3) 1997
show fluctuating flower temperatures that
are somewhat dependent on ambient temperature. However, there are three species
that produce remarkably constant temperatures in the face of fluctuating ambient temperature - they show a degree of temperature regulation.
Because flowers lack the complex nervous
thermoregulatory
features of animals, it is
apparent that regulation must occur at a cellular level and be triggered directly by
changes in flower temperature [6,7]. Indeed,
there is a progressive inhibition of heat production as flower temperature rises from 30
to 36°C (Figure 4).
The inhibition above 30°C is the key to
the thermoregulatory
mechanism. A stable
flower temperature will be attained at a
given environmental temperature if the rate
of heat production equals the rate of heat
loss. As a starting point, let us assume that
air temperature is 20°C and the flower has
warmed to 31°C (Figure 4). The difference
in temperature is 11°C and the rate of heat
production is about 550 mW. If the air
temperature
decreases
to lO” C, heat
loss increases
and flower temperature
decreases.
But when the flower falls
to 3072, its rate of heat production rises
to about 1000 mW and a new equilibrium
between heat loss and heat production
is reached. Conversely, if air temperature
rises to 3O” C, heat loss decreases and the
flower warms to equilibrium at 34°C and
produces about 280 mW. Thus the flower
temperature can move up and down the
slope, between 30 and 36”C, while the
environmental temperature varies between
10 and 45°C.
ering heat production, which continues during the day. Thus, at the same flower temperature, say 32”C, the rate of heat production can be 280 mW at 19.00 in the evening,
but 880 mW at 8.00 the next morning. Such
a marked hysteresis is indicative of ~10~
regulatory changes, possibly through alterations in concentration of regulatory biochemical intermediates or enzymes, rather
than structural changes in membranes or
enzymes.
Other thermoregulating plants
Environmental temperature (“C)
Figure 2 Relationship between flower temperature and ambient temperature in three
species of thermoregulating
plant. The lines are linear regressions from original data
[7,10,11].
and
P. Schultze-Motel,
unpublished
data).
A clue to the mechanism of temperature
regulation is a marked hysteresis in the relationship between rate of heat production
and flower temperature (Figure 5). As air
temperature drops quickly at night, it can
draw flower temperature
quickly from
about 36 to 30°C. Despite this temperature
decrease, heat production does not increase
for an hour or two. Eventually, the rate of
heat production rises throughout the night
as ambient temperature slowly declines.
When the sun first strikes the flower in the
morning, its temperature can rise quickly.
This often causes a huge spike in heat production before the flower responds by low-
The cause of this metabolic inhibition
above 30°C is not clear, but it is known that
it is completely
reversible.
Because
temperature regulation in Nelumbo occurs
over a few days, flowers that are inhibited
by high ambient temperatures during the
day become uninhibited at low temperatures
during the following night. It is also clear
that the response is directly related to flower
temperature, not some other environmental
cue such as light cycle. Flowers covered by
a translucent water jacket, in which high
temperatures are produced during the night
and low temperatures during the day, show
high rates of heat production when ambient
temperature is low, regardless of whether
it occurs during night or day (R.S. Seymour
800..
.g
600..
4
g
400..
5
2
200..
1 T
f
f
f
f
01
0
1
5
10
15
20
25
30
35
Ambient temperature (“C)
Figure 3 Rate of heat production in relation to ambient temperature during the
thermoregulatory
period of the sacred lotus Nelumbo nucifera. (Data from [7].)
40
45
The first plant shown to thermoregulate was
an arum lily, Philodendron sellourn (81. The
flowering sequence of its inflorescence (a
structure composed of many small flowers)
occurs over a two-day period, beginning as
the spathe opens widely to reveal the
creamy-white
spadix (Figure l(d)). The
onset of heating can occur during the day or
night, but high temperatures are maintained
for 18-24 hours, when the female florets are
receptive to pollination. In Brazil, the pollinators are l-2 cm scarab beetles, Erioscelis
emarginata [9]. A single flower can attract
hundreds of the beetles that mate within it
and feed on its floral parts and secretions.
As the spadix cools, the spathe closes
around it, trapping some beetles inside.
After about 12 hours, when the female
florets have been pollinated, the spathe
reopens and the fertile male florets shed
their pollen on the escaping insects. The
plant ensures that the beetles carry the
pollen away, because the spathe coats them
with a yellow sticky fluid and, by opening
only partially, it forces them to climb
through the pollen on their way out. When
they are released, there is a minor episode of
heating, but the beetles fly off with their
pollen loads to warmer plants with receptive
female florets. Cross-fertilization
is further
promoted because the inflorescences on a
given plant progress through the entire
sequence one at a time.
Unlike the lotus which demonstrates
exceptionally
tight
regulation,
Philodendron selloum exhibits less stable temperatures during its initial thermogenic
period. Nevertheless, its temperatures are
high, 3542°C in the field [9]. In the laboratory, intlorescences can warm to 39”C,
even at air temperatures as low as 4°C
(Figure 2) [Xl. Most heat is produced by
sterile male florets that cover the spadix
between the fertile male and female florets.
Experiments with sterile florets cut from the
spadix show that the flower thermoregulates
at the cellular level, by a steep, reversible,
thermal inhibition that occurs between 37
and 46°C [lo], a similar pattern as in the
lotus, but with a higher set-point.
A third thermoregulating
flower which
has a lower set-point than the lotus is the
eastern
skunk cabbage,
Symplocurpus
foetidus, also a member of the Araceae [ 111.
This plant blooms in early spring in North
America, and its inflorescence sometimes
melts a hole through ice or snow. The spadix
inside a leathery. cowl-shaped spathe emits
Endeavour
Vol. 21(3)
1997
127
temperature change (for example, Figure 5).
These similarities suggest a common, rather
sluggish, biochemical control mechanism.
1000
T
z
Evolutionary significance of
thermogenesis
800- -
g
6 600- '=
2
w
, o 400- Q
irj
I"
200- -
0'
0
I
I
I
I
I
10
20
30
40
I
50
Flower temperature (“C)
Figure 4 Diagrammatic view of the rate of heat production in
in the sacred lotus Nelumbo nucifera. Above about 3o”C, there
inverse relationship between heat production and temperature.
stable at the indicated points when the rates of heat production
(Data based on [7].)
a foul-smelling
odour that attracts beetles
and flies [12]. The pattern of temperature
changes throughout the two-week life of the
protogynous flower has not been measured,
but opportunistic
data indicate a strong
of temperature
independence
degree
between spadix and air. At air temperatures
of lS” C, the spadix averages about 24°C; if
air is -15°C the spadix can be 15°C (Figure
2). Recent data show a hysteretic delay in
responses to ambient temperature change;
for example, if snow is packed around the
inflorescence,
its temperature
drops ini-
relation to flower temperature
is a steep, reversible,
Flower temperatures are
and heat loss are equal.
tially, but then recovers in about one hour
(R.M. Knutson, personal communication).
The three species of thermoregulating
plants for which we have data (the South
American aroid Xanthosoma robusturn is
also said to thermoregulate [2]) share certain physiological features: (1) a small, but
significant, dependence of flower temperature on environmental temperature (Figure
2); (2) an inverse relationship between the
rate of heat production and ambient temperature (for example, Figure 3); and (3) a
pronounced delay in response to ambient
800 . '
. s 600 . .
5
4
g 400.
n
3
2
-
200.
0'
26
18:00
L
i5:OO
I
28
30
32
34
36
38
40
42
Flower temperature (“C)
Figure 5 Hysteresis in rates of heat production by sacred lotus Nelumbo nucifera at hourly
intervals during the circadian cycle. Open symbols indicate rising, and filled symbols
indicate falling, ambient temperatures. High temperatures during the day are unnatural,
resulting partly from solar heating in a respirometry hood. (Data from [7].)
128
Endeavour Vol. 21(3) 1997
From the foregoing it is apparent that
thermogenic
flowers are always protogynous and most heat production coincides
with the period of female receptivity.
Furthermore,
the important
pollinating
insects
are often beetles.
Gottsberger
]13,14] and others have made a convincing
case that the origin of the flowering plants
(angiosperms) involved a strong nexus with
beetle pollinators. It is significant that the
evolutionary
radiations
of thermogenic
plants and beetles coincide in the Mesozoic
era. Thermogenic
families appear only
among ancient groups of seed plants,
according to most systematists including
Chase et al. [15]. Cycads (Cycadaceae)
diversified in the Jurassic period and then
the angiosperms,
including
paleoherbs
(Nymphaeaceae
and Aristolochiaceae),
primitive monocots (Araceae, Arecaceae
and Cyclanthaceae),
basal woody dicots
(Annonaceae and Magnoliaceae), and lotus
(Nelumbonaceae),
diversified
in the
Cretaceous. The lotus family, the only eudicot, is the highest on the phylogenetic tree.
Among beetles, the first radiation also
occurred during the Jurassic, and it was followed by an explosive diversification in the
Cretaceous [16].
The morphology of many thermogenic
flowers seems well adapted for beetle pollination. Characteristics of ‘beetle flowers’
include large size, an internal chamber,
large number of widely spaced carpels with
exposed stigmas, flower parts offered as
food, and prodigious production of pollen
on numerous anthers. Flower scents in
ancient angiosperms are often matched to
the predilections of beetles searching for
places to feed, mate or lay eggs, and it is
thought that some fragrances
have coevolved with beetles to induce specific
activities [17]. Beetles in general are not
very manoeuvrable in flight and land clumsily, so the flowers often provide a broad
landing platform. Some fossil cycads, for
example, had bisexual cones surrounded by
horizontal bracts that would have provided
good landing places for them [16]. The
spathes, petals or bracts of angiosperms also
facilitate
alighting
and orientation
of
beetles.
Our contribution to this discussion lies in
pointing out the correlation between the
thermal requirements
of beetles and the
temperatures
maintained
inside thermogenie flowers. Many beetles are endothermic and require high temperatures in their
thoracic muscles for activity such as flight
[ 181. Minimum thoracic temperatures in
flight range from 27 to 34°C in scarab beetles weighing about 1 g (19-211. Even in
species weighing less than 200 mg, flight
temperatures are in the region of 25-35°C
[22]. In addition to flight, other activities
involved with intense competition for mates
and food require elevated body temperature
[21,23,24].
Because beetles are generally small and
not well insulated, they lose body heat
quickly, so they must expend large amounts
of energy to remain warm in a cool environment [lg]. Based on estimates of energy
expenditure of a 1.3 g scarab beetle maintaining a temperature elevation of a few
degrees above air [19], the animal would
have to eat about 100% of its bodyweight
each day. Without endothermy, its energy
requirement would be only 2.5% of the
body weight.
While many flowers reward their pollinators with energy rewards in the form of
nectar, pollen or starch, thermogenic flowers may augment the reward by the direct
application of heat. It is noteworthy that the
temperatures often found in thermogenic
tlowers are in the same range as those preferred by active beetles. Temperatures in the
floral chamber of Victoria amuzonica, for
example, are maintained
in a range of
26-32°C throughout the 23-hour period that
the scarabs (Cyclocephala sp.) are in residence
and feeding
on the flower
[4].
Temperatures
in the
South
American
Annonu
coriucea,
reach
custard
apple,
about 34°C on two successive nights; on the
first night Cyclocephala beetles meet in the
flower and copulate avidly, and on the
second night they are sprinkled with pollen
and prepared for their abrupt departure with
high body temperatures [25]. Philodendron
selloum inflorescences
remain in the region
of 28-44” C during the initial night of female floret receptivity when scarab beetles
(Evioscelis) are attracted (9,101. Nelumbo
nuciferu
tlowers thermoregulate
between
about 30 and 36°C when they are receptive
to pollination
[6,7], and attract cantharid
beetles (Chauliognathus) and bees [S].
Of course, evolution has not given a
monopoly to beetles for pollination of thermogenic flowers. In addition to beetles,
many arum lily species now attract flies and
small bees [12], insects that may be too
small to thermoregulate physiologically and
therefore are adapted for activity at lower
body temperatures. It is perhaps important
that plants pollinated by flies or smaller
insects produce very little heat and fail to
warm very much.
We propose that some thermogenic plants
evolved temperature regulation as a reward
to the insects that visit them. A warm, stable
temperature
might enhance locomotion,
digestion, growth, reproduction or access to
mates. Unfortunately, we do not yet understand the influence of a flower’s warming
on the well-being of its pollinators. Nor do
we know whether the warmth is a strict
requirement for survival or proper physiological function.
There have been no
measurements of the effects of temperature
on behaviour, reproduction or physiology of
any natural pollinator of a thermogenic
plant. Previous work has concentrated only
on the responses of the flowers, and our
studies have been confined to plants outside
their natural range, so the native pollinators
are absent. We are hopeful that future
research will include studies on the thermal
and energetic interactions
between both
partners in the phenomenon.
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