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42Evolution

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Are plants warm-blooded?

Dead-horse arum (Helicodiceros muscivorus) (Image: Ingemar Johansson/Wikimedia Commons)

Dead-horse arum (Helicodiceros muscivorus) (Image: Ingemar Johansson/Wikimedia Commons)

No, don’t be ridiculous

Picture the scene. “Darling, I’ve been a perfect fool”.  The acceptance – albeit with a curt nod – of a bouquet of flowers is promptly followed by a shriek: “You b*****d, they’re hot and the smell is appalling ….”.  Understandable in the heat of the moment, but why has the planned reconciliation gone pear-shaped?  Warm-blooded plants?  Granted plants and animals aren’t totally different.  Both have vascular systems, although rather than transporting blood it is the flow of water (in the xylem) and sugary fluids (in the phloem) that nourish the plant.  Sex may be seldom out of our minds, but it still comes as a shock to see flowers as merely beautiful genitalia.  Perhaps as disturbing is to listen to plants chatting as they exchange chemical information and warnings.  Some people talk about plant “intelligence”, but one has to draw the line somewhere.  Hot plants?  About as likely as a flying kangaroo.

Yes, of course

What is that horrific odour wafting through the air? Rotting carcasses, dog poo, cat pee are only some of the unexpected smells you can encounter in a stroll through the glades.  Swiftly you change direction, but not the insects.  They are making a proverbial bee-line towards the source of corruption.  Anticipating some noisome discovery the source of the volatiles are actually plants, engaged in ingenious chemical trickery in order to recruit pollinators.  As the insect approaches other forms of mimicry come into play with vivid pustules and lurid purples providing further encouragement.  So far as the volatiles are concerned, not all smell repulsive.  Some are sweet, and others are disarmingly similar to insect sex-pheromones.

But how to disperse these fragrances more rapidly and when the insects arrive ensure a comfortable and truly enjoyable visit?  The answer is simple: turn yourself into a natural radiator.  The trick of developing heat-generating tissue has evolved many times, not only amongst the flowering plants but also the one-time companion of the dinosaurs, the cycads.  Curiously amongst the former many are relatively primitive and include the sacred lotus, magnolias, palms, but especially the arum family (botanists salute the Araceae).  Given their propensity to emit pungent volatiles it is little surprise they end up with names like the Skunk cabbage and Dead-horse arum.  Some thermogenic plants are also enormous, such as the 3-metre-tall titan arum, not to mention the immense flowers of the parasitic Rafflesia that erupts from its host in the depths of the Sumatran jungle.  The signal to rack up the heat depends on salicylic acid (the cure for headaches), but there is a diversity of ways in both the amount of heat generated and the timing.  In some species the increase in temperature is a modest degree or two, but in one arum (Philodendron) the temperature can reach a whopping 46oC.  Occasionally the “furnace” runs uninterrupted for days and remarkably as the surrounding temperatures fluctuate so the plant regulates its own temperature.

More often there are discrete bursts of thermogenic activity, coinciding with different stages in the plant’s flowering.  To keep the metabolic fires burning the plant needs plenty of oxygen but lacking lungs this might seem a bit of a challenge.  Not really, because an abundance of tiny openings (stomata) allow the vital gas to diffuse into the thermogenic tissues.  Species by species the details differ, but a recurrent method is to release a blast of warm volatiles to bring the visitors flocking in.  Flies lead the rush, but beetles show an inordinate fondness for thermogenic palms and magnolias.  The central objective is to ensure the visitors fertilize the female flowers and/or arrange things so that the departing guests receive a dusting of pollen before they fly off in search of more female plants.  In Australian cycads one set of volatiles attracts thrips to the pollen, but a different blast sends them off in search of a female flower.  Not infrequently the timing between pollen production and female receptivity requires a temporary imprisonment in a floral chamber, but if so the insect’s time is not necessarily wasted.  In the toasty-warm environment they can take the opportunity to mate, lay eggs or feed on tissue thoughtfully provided by the plant.  Some plants recruit a variety of pollinators, but in other cases only a single species of insect will serve making animal and plant utterly interdependent.  Heat can also assist the plant, especially with early flowering when snow may cover the ground.  Without the warmth processes, such as pollen maturation, might otherwise be jeopardized.

It all depends on the question

My companion is mollified. “Well your “present” did take me by surprise.  What a story!  Isn’t it funny how evolutionary biologists find it so difficult to distinguish woods and trees?  It’s the general principles that matter”.  And that applies to any thermogenic organisms: plants, animals, even bacteria.  Usually the centre of activity are the respiratory organelles (mitochondria) and specifically the cytochrome-based electron transport chain that burns metabolic fuels (like sugars or fats).  Normally the resultant energy is stored in the ATP, but if this process (by so-called “futile cycling”) is derailed then heat is released.  In mammals, such “sabotage” depends on the aptly named uncoupling proteins (UCPs).  Plants use much the same mechanism, although to frustrate the normal respiratory pathway they usually employ AOX (alternative terminal oxidase).  Going full-pelt a thermogenic plant can produce as much heat as a flying hummingbird or sphinx moth.  In principle any tissue can produce heat, but flight muscles are a particular favourite.

In insects thermogenesis assists not only pre-flight warming (in bumblebees) and walking (for dung beetles), but even singing amongst the cicadas.  Although breezes, or for that matter gales, will strip an organism of its heat the challenges of living in water (where thermal conductivity is an order of magnitude greater) are more severe.  Whales opt for blubber, penguins for feathers, but a favourite trick is to devise a network of blood vessels (biologists speak in awe of the rete mirabile) so that heat making its way to the chilly extremities is clawed back to the warm interior.  Independently tuna and some sharks have devised this system and it is no accident that their thermogenic-based success allows them to dive deep into freezing waters and migrate rapidly across enormous distances.  In the billfish thermogenic muscles, recruited from ones that otherwise would swivel the eyeball, find a more extraordinary use.  When hunting in deep, cold waters not only does this enhance powers of vision, but by warming the brain it allows snap decisions rather than engaging in a glacial pondering.  The sunless ocean abyss seems a million miles from the Mediterranean islands where the Dead-horse arum disperses its repulsive scent, but the shared principles of thermogenesis warm the cockles of the scientific heart.

Text copyright © 2015 Simon Conway Morris. All rights reserved.

Further reading
Albury, M.S. et al. (2009)  Towards a structural elucidation of the alternative oxidase in plants. Physiologia Plantarum 137, 316-327.
Angioy, A-M., et al. (2004)  Function of the heater: the dead horse arum revisited.  Proceedings of the Royal Society of London, B 271 (Supplement), S13-S15.
Barthlott, W. et al. (2009)  A torch in the rainforest: thermogenesis of the Titan arum (Amorphophallus titanum). Plant Biology 11, 499-505.
Bartholomew, G.A. and Casey, T.M. (1977) Endothermy during terrestrial activity in large beetles. Science 195, 882-883.
Bartholomew, G.A. and Heinrich, B. (1978) Endothermy in African dung beetles during flight, ball making, and ball rolling. Journal of Experimental Biology 73, 65-83.
Bermadinger-Stabentheiner, E. and Stabentheiner, A. (1995) Dynamics of thermogenesis and structure of epidermal tissues in the inflorescences of Arum maculatum. New Phytologist 131, 41-50.
De Metrio, G. et al. (1997)  Heat-producing organ of the swordfish (Xiphias gladius): A modified eye muscle. Journal of Morphology 234, 89-96.
Fritisches, K.A. et al. (2005)  Warm eyes provide superior vision in swordfishes. Current Biology 15, 55-58.
Grant, N.M. et al. (2008) Synchronicity of thermogenic activity, alternative pathway respiratory flux, AOX protein content and carbohydrates in receptacle tissues of sacred lotus during floral development. Journal of Experimental Botany 59, 705-714.
Ito, K. and Seymour, R.S. (2005) Expression of uncoupling protein and alternative oxidase depends on lipid or carbohydrate substrates in thermogenic plants. Biology Letters 1, 427-430.
Ito, K. et al. (2011)  Identification of a gene for pyruvate-insensitive mitochondrial alternative oxidase expressed in the thermogenic appendices in Arum maculatum. Plant Physiology 157, 1721-1732.
Ito-Inaba, Y. et al. (2012)  The gene expression landscape of thermogenic skunk cabbage suggests critical roles for mitochondrial and vacuolar metabolic pathways in the regulation of thermogenesis. Plant, Cell and Environment 35, 554-566.
Lamprecht, I. et al. (2002)  Flower ovens: Thermal investigations on heat producing plants. Thermochimica Acta 391, 107-118.
Little, A.G. and Seebacher, F. (2014) The evolution of endothermy is explained by thyroid hormone mediated responses to cold in early vertebrates. Journal of Experimental Biology 217, 1642-1648.
Lytle, C.M. et al. (2002)  Oxygen-dependence of metabolic heat production in the appendix tissue of the voodoo lily (Sauromatum guttatum Schott). Thermochimica Acta 349, 135-140.
Miller, R.E. et al. (2011)  In the heat of the night – alternative pathway respiration drives thermogenesis in Philodendron bifinnatifidum. New Phytologist 189, 1013-1026.
Patiño, S. et al. (2002).  Is Rafflesia an endothermic flower? New Phytologist 154, 429-437.
Pereira, J. et al. (2014) Philodendron adamantinum (Araceae) lures its single cyclocephaline scarab pollinator with specific dominant floral scent volatiles. Biological Journal of the Linnean Society 111, 679-691.
Raskin, I. et al. (1989)  Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid.  Proceedings of the National Academy of Sciences, USA 86, 2214-2218.
Sanborn, A.F. et al. (2003)  Hot-blooded singers: endothermy facilitated crepuscular signaling in African platypleurine cicadas (Hemiptera: Cicadidae: Platypleura spp.). Naturwissenschaften 90, 305-308.
Seymour, R.S. (2004) Dynamics and precision of thermoregulatory responses of eastern skunk cabbage Symplocarpus foetidus. Plant, Cell and Environment 27, 1014-1022.
Seymour, R.S. (2010) Scaling of heat production by thermogenic flowers: Limits to floral size and maximum rate of respiration. Plant, Cell and Environment 33, 1474-1485.
Seymour, R.S. et al. (2003)  Environmental biology: Heat reward for insect pollinators. Nature 426, 243-244.
Stensmyr, M.C. et al. (2002)  Rotting smell of dead-horse arum florets. Nature 420, 625-626.
Suinyuy, T.N. et al. (2013)  Patterns of odour emission, thermogenesis and pollination activity in cones of an African cycad: what mechanisms apply? Annals of Botany 112, 891-902.
Tabata, K. et al. (2013)  Measurement of soil bacterial colony temperatures and isolation of a high heat-producing bacterium. BMC Microbiology 13, e56.
Terry, J. et al. (2007)  Odor-mediated push-pull pollination in cycads. Science 318, 70.
Watanabe, Y.Y. et al. (2015)  Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes.  Proceedings of the National Academy of Sciences, USA 112, 6104-6109.
Wegner, N.C. et al. (2015)  Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348, 786-789.

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