Hot termites, cold fungi, warm sharks

Termite nest in a dead Banksia, by Margaret R Donald [Creative Commons Attribution-Share Alike 4.0 International license].

A few plants, such as Amorphophallus species (Cyrille Claudel et al.) and Arum maculatum (Anneke Wagner et al.), are dramatically thermogenic with the capacity to increase their temperature well above that of their surroundings. Although those ‘horticultural hotties’ may hog the limelight when it comes to plants and their ability to regulate temperature, the more this phenomenon is investigated, the more common phytothermoregulation seems to be (Emily Litvack – a commentary on Sean Michaletz et al.). One of the commonest mechanisms plants employ for keeping cool is the evaporative cooling that occurs when water is lost through their stomata in the phenomenon known as transpiration (Agne Zenkeviciute). But what about fungi? With no stomata to help them, you might assume that their temperatures would be the same as their surroundings. Well, and somewhat surprisingly, some fungi can actually generate ‘body’ temperatures that are lower than their surroundings.

Like many of the best discoveries in science, this was found by accident (Vanessa Allnutt et al.; Adam Cole; Lexi Krock). In this instance, according to Bob Yirka, one of the quartet – of Radamés Cordero, Ellie Rose Mattoon, Ramos Zulymar & Arturo Casadevall – that reported this finding was testing a new thermal camera while isolating at home during the early days of the COVID-19 pandemic. The outcome of that ‘playing around’ was the discovery that a range of mushrooms were 2.9 ± 1.4 °C colder than the air surrounding them (Bob Yirka). As surprising as those results were, even more intriguing was the finding that the cooling effect was also found in mo(u)ld and colonies of unicellular yeast.

This finding reinforces the view previously proposed by Justin Husher et al. [whose work they acknowledge], that such fungal temperature-lowering behaviour is a result of ‘evaporative cooling’ [like the plant’s transpirational effect only without stomata]. But, Cordero et al. develop the notion to suggest that the phenomenon could be exploited for the benefit of humans in systems such as air conditioners or coolers (Seraiah Alexander). That potential use is fine so long as the system designed doesn’t encourage the dispersal of fungal spores – that may irritate or harm the humans (WG Sorenson; Jen Christensen) being kept cool [Ed. – which reproductive-assistance was one of the proposed biological values of this capacity explored by Husher et al.]. Nevertheless, and irrespective of whether such fungal fears can be forestalled, this work is official confirmation that fungi – despite not being plants but which are dealt with in a similar way from a taxonomic nomenclatural point of view, and which is good enough for Mr P Cuttings – are cool (David Skinner).

It surely won’t have escaped the notice of Botany One’s readers that global temperatures have been rather elevated of late – and that for a short period in July 2023 the Earth set an unofficial heat record (Seth Borenstein). Although the planet may – or may not – have been this hot within the last 100,000 or 120,000 years (Darrell Kaufman), it was certainly very warm and focussed humanity’s attention on global warming (Amanda MacMillan & Jeff Turrentine). However, of all the phenomena associated with globally-elevated temperatures, perhaps one of the most unanticipated is the effect that this might have on the feeding behaviour of termites (Kumar Krishna). Termites are insects probably most well-known for their ability to eat wood (despite famously being unable to digest this plant-derived food source without the biochemical assistance of intestinal tract-located partners (Mary Sharp)).

Investigating the wood-chomping activity of termites, Amy Zanne et al. (>100 of them!) made an interesting discovery. Examining how quickly termites ate blocks of dead wood that had been left outside for at least a year in different regions with varying temperatures and rainfall, they found that the wood-degrading activity of these xylovores increased as temperatures increased. Termite decay effects were greatest in tropical seasonal forests, tropical savannas, and subtropical deserts. This led the team to conclude that with the planet’s progressive ‘tropicalization’ (i.e., warming shifts to more tropical climates) that accompanies global warming, termite-mediated wood decay will likely increase as termites access more of the Earth’s surface.

Should we be concerned by this revelation? Yes. Dead wood is a store of carbon (Marisa Stone et al.), and, if safely buried (Ning Zeng), or otherwise left alone, is a way of keeping that carbon out of circulation. However, dead wood that’s broken-down and decomposed – e.g. by termite activity – is a source of CO₂ into the atmosphere (Marisa Stone et al.), which contributes to additional global warming. And it gets worse.

Readers may be familiar with the concept of the temperature coefficient Q₁₀ (JRG Beavon). For (bio)chemical reactions, that value is approx. 2, i.e. the rate of reaction doubles for a 10^oC increase. Termite’s ‘biological’ Q₁₀ is substantially higher – at >6.8-fold (Zanne et al.) in the studied temperature range of 68 – 86^o Fahrenheit. Not only is that rate of breakdown even faster than wood-decomposition by termite-independent microbes, the enhanced release of CO₂ is likely to increase global warming.

Whilst dead wood in the open is fair game for termites, we should spare a thought for those whose homes are made of, or contain, dead wood, which is a food source famously exploited by termites (Ashley Dando). So, not only must we be mindful of global warming-associated wild fires (Daisy Dunne) destroying property – and sadly people as so tragically and devastatingly demonstrated on the Hawaiian island of Maui in August 2023 (Will Potter; Dani Anguiano), there’s the added complication of termite-induced destruction of wood-based buildings. Termites might be classified as ‘social’ insects (Thomas Harper; Matt), but their response to temperature increase appears to be distinctly antisocial.

We’ll finish this biothermobehavioural round-up with news of a fish that’s warmer than it should be – at least according to the textbooks. Basking sharks (Eddie Johnston & Lisa Hendry,* as a type of shark (Jeffrey Carrier), should be what we used to call ‘cold-blooded’ (Robert Hill; Sagar Aryal). That is to say their body temperature is supposed to be more or less the same as the ocean in which they swim, cooling as the water temperature drops, and increasing as the sea warms.

However, when this was actually investigated by Haley Dolton et al. they found that particular parts of the shark’s body had temperatures that were consistently 1.0 – 1.5°C above ambient. This phenomenon – known as regional endothermy – is believed to give fish that possess it – such as the bluefin tunny – an advantage in preying upon active but colder-temperature fish species (Carly Cassella). But, why passively-plankton-feeding basking sharks need this ability is not yet clear.** One thing’s for sure, the textbooks will need to be updated.

READ THE ARTICLES

Claudel, C., Loiseau, O., Silvestro, D., Lev-Yadun, S. and Antonelli, A. (2023) “Patterns and drivers of heat production in the plant genus Amorphophallus,” The Plant Journal: for cell and molecular biology. Available at: https://doi.org/10.1111/tpj.16343.

Cordero, R.J.B., Mattoon, E.R., Ramos, Z. and Casadevall, A. (2023) “The hypothermic nature of fungi,” Proceedings of the National Academy of Sciences of the United States of America, 120(19). Available at: https://doi.org/10.1073/pnas.2221996120.

Dolton, H.R., Jackson, A.L., Deaville, R., Hall, J., Hall, G., McManus, G., Perkins, M.W., Rolfe, R.A., Snelling, E.P., Houghton, J.D.R., Sims, D.W. and Payne, N.L. (2023) “Regionally endothermic traits in planktivorous basking sharks Cetorhinus maximus,” Endangered Species Research, 51, pp. 227–232. Available at: https://doi.org/10.3354/esr01257.

Husher, J., Cesarov, S., Davis, C.M., Fletcher, T.S., Mbuthia, K., Richey, L., Sparks, R., Turpin, L.A. and Money, N.P. (1999) “Evaporative cooling of mushrooms,” Mycologia, 91(2), pp. 351–352. Available at: https://doi.org/10.1080/00275514.1999.12061025.

Michaletz, S.T., Weiser, M.D., Zhou, J., Kaspari, M., Helliker, B.R. and Enquist, B.J. (2015) “Plant thermoregulation: Energetics, trait–environment interactions, and carbon economics,” Trends in Ecology & Evolution, 30(12), pp. 714–724. Available at: https://doi.org/10.1016/j.tree.2015.09.006.

Sorenson, W.G. (1999) “Fungal spores: hazardous to health?,” Environmental Health Perspectives, 107(suppl 3), pp. 469–472. Available at: https://doi.org/10.1289/ehp.99107s3469.

Wagner, A.M., Krab, K., Wagner, M.J. and Moore, A.L. (2008) “Regulation of thermogenesis in flowering Araceae: The role of the alternative oxidase,” Biochimica et Biophysica Acta. Bioenergetics, 1777(7–8), pp. 993–1000. Available at: https://doi.org/10.1016/j.bbabio.2008.04.001.

Zanne, A.E., Flores-Moreno, H., Powell, J.R., Cornwell, W.K., Dalling, J.W., Austin, A.T., Classen, A.T., Eggleton, P., Okada, K.-I., Parr, C.L., Adair, E.C., Adu-Bredu, S., Alam, M.A., Alvarez-Garzón, C., Apgaua, D., Aragón, R., Ardon, M., Arndt, S.K., Ashton, L.A., Barber, N.A., Beauchêne, J., Berg, M.P., Beringer, J., Boer, M.M., Bonet, J.A., Bunney, K., Burkhardt, T.J., Carvalho, D., Castillo-Figueroa, D., Cernusak, L.A., Cheesman, A.W., Cirne-Silva, T.M., Cleverly, J.R., Cornelissen, J.H.C., Curran, T.J., D’Angioli, A.M., Dallstream, C., Eisenhauer, N., Evouna Ondo, F., Fajardo, A., Fernandez, R.D., Ferrer, A., Fontes, M.A.L., Galatowitsch, M.L., González, G., Gottschall, F., Grace, P.R., Granda, E., Griffiths, H.M., Guerra Lara, M., Hasegawa, M., Hefting, M.M., Hinko-Najera, N., Hutley, L.B., Jones, J., Kahl, A., Karan, M., Keuskamp, J.A., Lardner, T., Liddell, M., Macfarlane, C., Macinnis-Ng, C., Mariano, R.F., Méndez, M.S., Meyer, W.S., Mori, A.S., Moura, A.S., Northwood, M., Ogaya, R., Oliveira, R.S., Orgiazzi, A., Pardo, J., Peguero, G., Penuelas, J., Perez, L.I., Posada, J.M., Prada, C.M., Přívětivý, T., Prober, S.M., Prunier, J., Quansah, G.W., Resco de Dios, V., Richter, R., Robertson, M.P., Rocha, L.F., Rúa, M.A., Sarmiento, C., Silberstein, R.P., Silva, M.C., Siqueira, F.F., Stillwagon, M.G., Stol, J., Taylor, M.K., Teste, F.P., Tng, D.Y.P., Tucker, D., Türke, M., Ulyshen, M.D., Valverde-Barrantes, O.J., van den Berg, E., van Logtestijn, R.S.P., Veen, G.F. (ciska), Vogel, J.G., Wardlaw, T.J., Wiehl, G., Wirth, C., Woods, M.J. and Zalamea, P.-C. (2022) “Termite sensitivity to temperature affects global wood decay rates,” Science (New York, N.Y.), 377(6613), pp. 1440–1444. Available at: https://doi.org/10.1126/science.abo3856.

Zeng, N. (2008) “Carbon sequestration via wood burial,” Carbon Balance and Management, 3(1). Available at: https://doi.org/10.1186/1750-0680-3-1.

* Unlike most sharks, these giant fish famously only eat plankton, a mix of unicellular plant- (phytoplankton (Patricia Glibert)) and variously-celled animal-like (zooplankton) organisms. Although they apparently prefer zooplankton, basking sharks do eat some phytoplankton (DC Demetre). Since they consume some photosynthetic material their feeding biology means they’re a legitimate subject for consideration in this blog item.

** At the risk of making readers feel a little uncomfortable, it is worth noting that basking sharks are similar to great white sharks in possessing regional endothermy. However, basking sharks are regarded as ‘gentle giants’ because of their diet, which doesn’t include humans – as may occasionally be the case for great whites (Brandi Allred; Richard Gray)(!).