Warm flowers, happy pollinators
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Warm flowers, happy
pollinators
We tend to regard insects as ‘cold blooded’ and plants as passively adopting the temperature
around them. Yet, a bumblebee’s body temperature can be above 40oC, and needs to be at
least 30°C for its flight motor to run smoothly. Flowers have invented a number of tricks
to cater to this need: they warm themselves (and thus the nectar they offer to the bees) to
several degrees above ambient temperature. The bees, in turn, use surprising strategies to
identify warmer flowers.
Heather Whitney1
T
he café in the botanic gardens at their temperature; as well as this being of
and Lars Chittka2 Cambridge is a wonderful place to developmental advantage to the flower it
1
sit on a cold, bright February day. could also act as an additional incentive
Cambridge From there you can watch the emerging for pollinator visits, much as the hot cup
University & 2Queen spring flowers, early bumblebees and pos- of tea is an additional incentive to visit
Mary, University of turing birds from the warmth, and a hot the warmth of the café.
London cup of tea sets you up well to face the brisk
Title image. Bees winds outside. However, the emerging Floral warmth
looking for floral warmth? spring flowers and their pollinators man- The ability to create a warm flower may
Bumblebee (Bombus age to cope in the spring chill without the well have arisen early in the evolution of
terrestris) foragers
exploring Van Gogh’s
warmth we so crave at this time of year. the angiosperms. Members of several ba-
Sunflowers (copy painted Or do they? We now know that flowers sal angiosperm families such as the Nym-
by Julian Walker). have a huge variety of ways of increasing phaeaceae and Magnoliaceae have the
Warm flowers | IOB
ability to actively produce heat in their have this feature, it is particularly prev-
flowers. The mechanism used is the alter- alent in flowers that occur in the Arctic,
native respiratory pathway, mediated by and could be seen as a particularly ‘arctic’
an enzyme – alternative oxidase (AOX) adaptation, as it allows the flower to fully
– that occurs inside the mitochondrial utilise the midnight sun that occurs in the
membrane. While this pathway occurs in far north. For the flowers of the arctic pop-
all plants (its usual role is thought to be py Papaver radicatum this adaptation can
the production of reactive oxygen com- increase the flower temperature by up to
pounds that are important for defence 6 degrees above ambient for 50% of their
against microbes), most plant species lives, which increases the number of days
appear not to take advantage of its abil- these flowers can actively grow by an extra
ity to produce heat. This capacity can be 25% (Kevan 1989). When the sun-tracking
considerable, heating tissues by over 35°C ability of the flower was artificially pre-
above ambient temperature in the case of vented, both the quantity and quality of
Philodendron selloum, an arum lily! In the seeds was reduced (Kevan 1989).
several species a lower but more constant The arctic poppy has another adapta-
temperature is preferred and respiratory tion that may help it in the harsh arctic
heat production is regulated to achieve conditions. The petal epidermal cells are
fairly constant flower temperatures in wide- ‘reversed papillate’. This means that the
ly variable environmental temperatures inner tangential epidermal cell walls have
(see references in Seymour et al, 2003). papillae (cells with a pronounced conical
However, the flowers that actively pro- shape) pointing into the internal cells of the
duce heat are relatively few. Other flow- petal. It is thought that these structures
ers rely on a more ‘passive’ method: they help to focus the light into these internal
make the most of the ambient sunlight cells, warming the petal and making the
by converting it into warmth. Many of the most of the heating ability of the light.
flowers that show the most effective adap- These ‘reversed papillate’ cells also occur
tations to increase floral warmth are Arctic in early spring flowers such as Crocus
or Alpine species, where low temperatures where increasing the floral temperature
can result in reduced seed production. In is important (McKee and Richards, 1998).
fact, flower temperature can be a greater Conical cells on the petal epidermis are
factor than pollinator visits in the amount very widespread – it has been estimated
of seed produced. Therefore a higher floral that 80% of angiosperm flowers have them
temperature is beneficial: it ensures pro- (see references in Dyer et al, 2007). They
tection of the flower during periods of cold, occur in a couple of different forms, the re-
stabilises floral development, helps with versed papillate form of Papaver and Cro-
pollen germination, ovule development, cus, and the external conical form where the
and may help pollen tube growth (Kevan cells project out from the petal surface (Fig-
1989). Features thought to increase floral ure 1). However, the extent to which these
temperature include flower shape, size cells can influence the temperature of the
and angle to the sun. flower has only recently been investigated.
One particularly effective feature is In 1994 Noda and colleagues from the
that of heliotropism, where the flower John Innes Centre, Norwich, identified a
consistently follows the sun. Although a snapdragon (Antirrhinum majus) mutant
range of flowers (for example sunflowers) that lacked conical cells. It was possible to
Figure 1. (a) Wild type snapdragon (Antirrhinum majus) flowers have a deeply saturated purple colour (left) while mixta mutant
snapdragons are pink (right). Both these flowers produce exactly the same floral pigments. It turns out that the only direct effect of the
mixta mutation is a change of shape in the epidermal cells, with indirect effects on both floral colour and temperature. (b) Scanning
electron microscope images of Antirrhinum petal surfaces: conical shaped cells of the wild type (left); flat cells of a mixta mutant petal
(right). The conical cells act as lenses to focus the light into the pigment-containing vacuoles.
a b
IOB | Warm flowers
identify them due to the fact that the mu- greater contrast with green of the darker
tant flowers were significantly paler than colour make it any easier for the bees to
those of the wild-type plants (Figure 1a). find the flower (Dyer et al, 2007). What
While the wild-type, magenta, Antirrhinum else about the effect of conical cells on the
flowers have conical petal epidermal cells, flowers could be attracting the pollinators,
those of this mutant, which appears paler- and leading them to choose conical-celled
pink in comparison, were found to be flat flowers over those with flat cells? Comba
(Figure 1). The pigments produced in both and colleagues also found that the snap-
the flower types are exactly the same; thus dragon flowers with conical cells were
it is the shape of the cells that leads to the significantly warmer than the flat-celled
difference in the colour we perceive. flowers (Comba et al, 2000).
The mutation was found to occur in the The snapdragon mixta mutant was
mixta gene, which encodes a transcription isolated due to the difference in colour it
factor. Transcription factors are required to showed from the wild-type snapdragon
activate specific genes, for example for de- flowers. The effects of colour and tem-
velopmental processes during the growth perature can be closely linked in flowers.
of a cell. The MIXTA transcription factor Conical cells are thought to act as lenses,
is required for the activation of directional focusing light into the epidermal cell vac-
cell expansion (Noda et al, 1994). In virtu- uoles that contain floral pigments such as
ally all cases, conical cells are only found anthocyanins (see references in Dyer et
on the petals of flowers, not the leaves, and al, 2007). It is easy to imagine how this
this restricted expression pattern has led ‘focusing’ effect of the conical cells could
to the suggestion that conical cells are affect both temperature and colour. The
produced to enhance the attractiveness of colour that animals perceive in an object
the flower to potential pollinators. The fact is a function of the light that the object re-
that the presence of these cells affects the flects – which is dependent on the incident
colour of flowers added weight to this sug- light minus the light the object’s surface
gestion – but could this be the only function absorbs. At the same time, of course, ab-
for conical cells? sorbed light is also converted into heat. In
To study the effect conical cells had on addition, temperature may influence the
pollinators, field experiments were carried production of pigments that result in floral
out on snapdragon flowers of both wild- colour. In several species that have a vari-
type and mixta flowers. Using these two ety of colours, a temperature difference
flower sets, which were genetically identical between different colours has been found.
except for the mutation in the mixta gene, However, there does not appear to be a
meant that the effect of a single trait on simple and consistent pattern in terms of
pollinator behaviour, in this case that of which flower colours are associated with
conical cells, could be observed. Both lots more warmth. In the arctic poppy P. radi-
of flowers had had their anthers removed catum, where two forms – white and yel-
(emasculated), to prevent self-pollination. It low – exist, the yellow flowers were found
was found that, under these conditions, the to be significantly warmer, which is what
mixta flowers produced much less seed than one might expect. White surfaces bounce
the wild-type. This was not the case when back (do not absorb) much of the incident
the flowers were pollinated by hand. light, whereas yellow flowers absorb some
So both sets of flowers were equally capa- light and might convert the light energy to
ble of producing seed if pollinated, and the heat. In Crocus, however, where three col-
only reason for the reduced seed set in the ours were studied, the purple and white
mixta flowers was due to a reduced visita- flowers were found to be warmer than
tion rate by pollinators (Glover and Martin the yellow flowers (McKee and Richards,
1998). Indeed, this was later observed in 1998). In general, one might predict that
greater detail – fewer bumblebees were ob- a darker flower would be warmer, but the
served visiting the mixta flowers when they yellow crocuses deviate from the predic-
were planted in randomly arranged plots tion that they should be warmer than the
with wild-type flowers (Comba et al, 2000). white flowers. Clearly, more data are need-
So conical cells do enhance the attrac- ed so that we understand whether there
tiveness of the flower to pollinators – but is is a general pattern linking flower colour
this only due to the effect on colour? Work and temperature, in such a way that pol-
done with flower-naïve Bombus terrestris linators might actually be able to antici-
bumblebees has shown that while bum- pate the temperature of a flower from its
blebees can tell the two flower types apart colour, without first having to probe it.
by colour, the bees do not show any innate Thus, pigmentation can have an influ-
preference for either colour, nor does the ence over temperature, but the reverseWarm flowers | IOB
may also be true. Flower pigmentation is Figure 2. Thermographic
controlled by a range of internal and ex- image of a bumblebee
on a flower taken with an
ternal factors, and one of these factors is infrared camera. Brighter
temperature. In petunia, a period of mod- colours indicate higher
erately-low temperature increases anthocy- temperature. Photo by
anin production and so enhances flower B. Bujok, M. Kleinhenz,
pigmentation (Shvarts et al, 1997). As a J, Tautz (Beegroup Würz-
burg), with permission.
darker flower would be warmer, this ‘uni-
versal stress response’ of anthocyanin pro-
duction (plants produce anthocyanins in
response to many stressful environmental
triggers) in this case may have the addi-
tional advantage of helping to ameliorate
the situation.
Responses of pollinators
Bees have spectacular thermoregulation
abilities and can raise their body temper- sometimes use warm flowers as shelters –
ature to 30oC above ambient temperature but can they also ‘forage for heat’ by pick-
to near 40oC (Figure 2). Indeed, they need ing warmer flowers in their typically brief
such high temperatures to be able to fly. visits during nectar collection? Social bees
They do this by shivering their flight mus- are the intellectuals of the insect world,
cles, but this takes a lot of energy (Hein- with outstanding learning abilities. Can
rich and Esch, 1994). Hence, a good strategy they learn to pick the warmer flowers, and
would be to obtain some of the heat from learn the cues that identify them from a
external sources. Warmer flowers are more distance?
attractive to pollinators. It has previously As discussed, in snapdragons a single
been observed that insects will bask on gene difference leads to a reduction in
warm, sunlit leaves or flowers. In Arctic floral temperature but also to subtle col-
flowers, warmer flowers were found to at- our change (Comba et al, 2000). In recent
tract more pollinators due to the use by laboratory experiments, the Antirrhinum
the insects of the flower as a heating site mixta/wild-type flower system was mim-
during low temperatures (Kevan, 1989). icked, using artificial flowers (Figure 3a)
Heat-producing flowers reward insects that were similar to those displayed by the
with a direct energy reward. This was wild-type and mixta flowers (pink and pur-
shown by some elegant research by Roger ple; Figure 1a). Equal amounts of ‘nectar’
Seymour and colleagues who studied Cy- were supplied on each artificial flower, but
clocephala colasi beetles, which are the while the pink flowers remained at room
main pollinators of the lily Philodendron temperature, the purple flowers were 8
solimoesense in French Guiana (Seymour degrees warmer. The bees were able to dis-
et al, 2003). The flower produces heat so tinguish the two temperatures, and pre-
that, at night, the floral chamber is 3.4-5.0 ferred to visit the warmer (purple) flowers
degrees warmer than the ambient temper- (Figure 3b). This means that bees can use
ature. Since the beetles have to produce floral colour as a cue to both distinguish
heat to keep their body temperatures high between flowers of different temperatures
enough for activity, beetles that remain in and then to discriminate against the cool-
a warm flower during the night use less er flowers (Dyer et al, 2006).
than half the energy they would have used These experiments show how bumble-
if they had stayed out in the open. bees cleverly reduce their own investment
Flowers that warm themselves by more in making heat by seeking out flowers
passive means can still use temperature with warmer nectar – they are essentially
as a heat reward. In Oncocyclus irises, the collecting warmth, because warmer nectar
very dark floral colour of the flower con- constitutes a direct metabolic reward.
tributes to the floral microclimate such This discrimination against cooler flowers
that the flower is 2.5 degrees warmer than could be the reason why the mixta mutant
the ambient night temperature. The pol- flowers were avoided by pollinators in
linators of this flower, male solitary bees, the field trials: having sampled both the
shelter in the flowers and are able to use cooler flat celled flowers and the warmer
this additional warmth to start foraging conical flowers the bees actively chose to
earlier than those kept at a lower temper- visit only the warmer flowers, which they
ature (Sapir et al, 2006). could distinguish using flower colour as a
These observations show that insects cue. These results suggest that warmth isIOB | Warm flowers
a b
65
60
Preference (%)
55
50
45
40
35
30
21 21 29 21
Temperature (deg C)
Figure 3. (a) A bumblebee worker imbibing sucrose solution from an artificial flower in a laboratory flight arena. Artificial flowers were
made from plastic tubes with painted lids, and a small nectar reservoir glued onto the top. Water inside the tubes allowed to stabilise
the temperature of the flowers (Photo by A G Dyer); (b) Bees preferred the warmer purple flowers over the cooler pink flowers (right pair
of columns) – but this preference was not apparent when the flowers were equal in temperature (left two columns). This shows that the
preference for purple was not innate, but had to be learnt in conjunction with the temperature difference.
a significant factor in both the attraction warmth as an indicator of nectar produc-
and retention of a pollinator to a flower tion might not necessarily be a particularly
species, and could therefore be important reliable cue, and choosing warmer flowers
in the maintenance of floral features in for their metabolic reward of heat alone
the economy of nature. would provide sufficient motivation for a
chilly pollinator.
Scent and nectar production
Warmer flowers may also increase the at- Conclusions
tractiveness of a flower from a distance by Flowers have a wide array of ways to attract
enhancing the evaporation of floral scents. and reward pollinators. The complex fac-
In the case of the flowers heated actively tors linking temperature as both a reward
by the alternative respiratory pathway, and a cue, as well as its influence on other
it has been found that the temperature rewards and cues is gradually being under-
was important in attracting pollinators stood. However, it is good to know as you
by olfaction. Work by Angioy et al (2004) observe the activity of bumblebees from
on the thermogenic flowers of dead horse the warmth of a café, that as well as get-
arum (Helicodiceros muscivorus) showed ting food from their mutualist partners,
that the effect of heat on oligosulphide the bees are also getting warmth. A warm
volatiles was important in attracting blow flower and a hot sweet drink – what more
flies, the pollinators of this plant. As heat could any chilly pollinator ask for? What
is also an important oviposition cue for the bees appear to be doing is indeed a bit
blow flies, temperature itself may again be like us drinking a hot drink on a cold day.
an important cue in this plant-pollinator If you need to warm up, you can produce
interaction, as well as influencing other your own heat, at the expense of some of
cues such as volatiles. As discussed below, your energy reserves - or you can consume
warmer flowers usually produce more nec- a warm drink, and save on investing your
tar of greater quality, so an ability to use own energy. A fascinating observation is
temperature as a cue would be an advan- that bees do not just prefer the warmer
tage to potential pollinators. drinks – they also learn to predict the
Nectar production is a temperature de- flower temperature from the flower colour.
pendent biological process, and investiga-
tions have found that at low temperatures
nectar secretion in most species decreases References
(Corbet, 1979). This could mean that if a Angioy A M et al (2004) Function of the heater: the
flower is warmer it could constitute a bet- dead horse arum revisited. Proceedings of the
Royal Society Series B-Biology Sciences 271: S13–
ter source of nectar, which would act as S15.
an additional incentive for pollinators to Corbet S A (1979) Post-secretory determinants of
choose warmer flowers. However, nectar sugar concentration in nectar. Plant, Cell and En-
production is hugely variable, even within vironment 2: 293-308.
Comba L et al (2000) The role of genes influencing
the same plant individual, and is subject
the corolla in pollination of Antirrhinum majus.
to many environmental factors. Thus, Plant, Cell and Environment 23: 639-647.Warm flowers | IOB Dyer A G et al (2007) Mutations perturbing petal Noda K et al (1993) Flower colour intensity depends cell shape and anthocyanin synthesis influence on specialized cell shape controlled by a Myb-re- bumblebee perception of Antirrhinum majus lated transcription factor. Nature 369: 661-664. flower colour. Arthropod-Plant Interactions DOI: Sapir Y, Shmida A and Ne’eman G (2006) Morning 10.1007/s11829-007-9002-7 floral heat as a reward to the pollinators of the Dyer A G et al (2006) Behavioural ecology: Bees asso- Oncocyclus irises. Oecologia 147: 53-59. ciate warmth with floral colour. Nature 442: 525. Seymour R S, White C R and Gibernau M (2003). Glover B J and Martin C (1998) The role of petal cell Heat reward for insect pollinators. Nature 426: shape and pigmentation in pollination success in 243-244. Antirrhinum majus. Heredity 80: 778-784. Shvarts M, Borochov A and Weiss D (1997) Low tem- Heinrich B and Esch H (1994) Thermoregulation in perature enhances petunia flower pigmentation bees. American Scientist 82: 164-170 and induced chalcone synthase gene expression. Kevan P G in Mercer J B (ed.) Thermal physiology Physiologia Plantarum 99: 67-72. (1989). Proceedings of the International Symposi- um on Thermal Physiology, Tromsø, Norway, 16-21 July 1989. Amsterdam: Elsevier Science Publish- Heather Whitney is a Postdoctoral Researcher at the Department ers BV. (Biomedical Division). 747-753. of Plant Sciences, University of Cambridge, Downing Street, McKee J and Richards A J (1998) Effect of flower Cambridge CB2 3EA. structure and flower colour on intrafloral warming Lars Chittka is Professor of Sensory and Behavioural Ecology and pollen germination and pollen-tube growth in at the School of Biological & Chemical Sciences, Queen Mary, winter flowering Crocus L. (Iridaceae). Botanical University of London, Mile End Road, London E1 4NS. Email: Journal of the Linnean Society 128: 369-384. l.chittka@qmul.ac.uk IOB Members’ Evening Osteoporosis and Space Speaker: Adam Hawkey Thursday 18 October, 6.15pm to 8.30pm at the IOB £10 Members, includes light refreshments. There are 35 places for this event which carries 5 IOB CPD Credits Adam Hawkey is a Lecturer with in the Research Centre for Sport, Exercise and Performance at the University of Wolverhampton. He has research experience with the National Aeronautics and Space Administration’s (NASA) Biomedical Task Group, investigating the effectiveness of exercise training protocols for human space flight. He has also been involved in the British Interplanetary Society’s Mars Polar Base project. He currently advises the National Space Science Centre on human spaceflight issues and recently acted as Scientific Consultant on a special ‘IMAX-style’ feature entitled “Astronaut”. His current research is now firmly focused on establishing the effects of low magnitude, high frequency signals (vibration) on a variety of health and performance related issues. These include: bone mineral density for osteoporosis and rheumatoid arthritis sufferers, dancers, and astronauts; jump performance for basketball players; and power output for sports performers. For more information please contact: Annaliese Shiret, Events and Conference Manager, 9 Red Lion Court, London, EC4A 3EF. Tel: 020 7936 5980 INSTITUTE Email: a.shiret@iob.org OF BIOLOGY
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