Very early on in study of the natural world one comes to realise that Charles Darwin’s ‘fingerprints’ are seemingly everywhere: Many aspects of biology that are studied today draw upon – or are related to – previous work of the venerable Mr D. In plant biology we are fortunate to have many instances where his influence is present. For example: insights into plant growth and development and its regulation by hormones (William Gray), discovery of which compounds was anticipated by work [with his son] on light-induced coleoptile curvature; the debate about plant intelligence (Paco Calvo et al.; Jennifer Khattar et al.; Umberto Castiello), which often cites Darwin’s notion of a root-brain (Paco Calvo Garzón & Fred Keijzer); investigations into the dramatic increase in angiosperm diversity during the Cretaceous (Michael Dhar) period (Hugo de Boer et al.) still refer to Darwin’s ‘abominable mystery’ (Frank Berendse & Marten Scheffer; William Friedman) [and here we shouldn’t forget his highly influential contribution to views on evolution by natural selection more generally]; the extraordinary biology of carnivorous plants (e.g. Dale Maylea) frequently examines Darwin’s “most wonderful plants in the world”; the importance of earthworms to soil and the relevance of this growth medium to (plant) ecology; the increasingly recognised importance of study of plant pollination, which can be related to Darwin’s own interests in the fertilisation of orchids (Claire Micheneau et al.; Andrea Cerase).
So much for terrestrial phenomena, but his interests didn’t stop on dry land. Darwin also contributed much to the biology and natural history of the oceans. His monumental study of barnacles aside [because that’s far too zoological for a plant-focussed blog item], Darwin had quite a lot to say about coral reefs, e.g. his hypothesis regarding the formation of coral atolls. Although that mechanism is now disputed (Alexandra Witze; André Droxler & Stéphan Jorry), Darwin’s legacy has not been ignored. Neverthelss, coral reefs are relevant to a Plant Cuttings piece because at the heart of that entity is the intimate association between a photosynthetic alga – termed a zooxanthella – and its animal host, the coral polyp. And one of the most intriguing of the great man’s musings on this ecosystem is known as Darwin’s paradox of coral reefs (Francis Rougerie).
This paradox concerns the conundrum in which high productivity of warm-water coral reefs* exists – and is maintained – even though they are surrounded by an otherwise productively-poor ocean. How is this possible? Amongst the scientists intrigued by this ‘anomaly’** are Jörg Wiedenmann et al., who think they may have solved the mystery.***
In a nutshell, Wiedenmann and colleagues’ work looked specifically at the mechanisms whereby the essential nutrients nitrogen and phosphorus are acquired by the coral. They discovered that these nutrients are actually gathered through ‘symbiont farming’ and are transferred to the polyp host by digestion of cells of its algal partner. Although this may look like a case of ‘biting the hand that feeds you’, the host only appears to digest excess symbiont cells – and the overall integrity of the symbiosis is retained. Wiedenmann et al. end the abstract (Suhasini Nagda) of their study with this neat conclusion: “Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters”.****
However, is the puzzle really solved? Is this 2023 research on Darwin’s Paradox the end of the story? One would like to think so, but I am moved to ask the question because this curious and captivating coralline conundrum has supposedly been solved several times before. For example, in 2013 the answer was sponges, and the phenomenon known as the ‘sponge loop’ – according to work by Jasper M. de Goeij et al. In 2014 “a study shows coral polyps actively generate micro-currents and eddies to promote nutrient inflow and exchange of materials using externally located cilia“. It was confidently claimed in 2016 that “Scientists solve ‘Darwin’s Paradox’”, and that was down to the Island Mass Effect (IME) as described by Jamison Gove et al. who investigated the phenomenon of “near-island biological hotspots in barren ocean basins”. A slightly more cautious headline from 2019 announced that “Researchers may have solved Darwin’s Paradox of how reefs are so productive” (Brian Kahn). That year, ‘flavour of the month‘ was cryptobenthic fish (Christopher Goatley & Simon Brandl) which fuel production of fish within the coral reef by providing an extensive supply of their larvae from the environment beyond the reef (Simon Brandl et al.). Maybe, the 2023 study is merely the latest in a long line of attempts to resolve the riddle but hasn’t yet solved it. Widenmann and colleagues’ work may therefore just be a case of ‘paradox postponed’.
But, a coral reef isn’t only about the coral symbiosis, it’s a much bigger, diverse community than that. So, maybe sponge loops, ciliary movement by polyps, the IME, cryptobenthic fish, and polyps farming zooxanthellae [and other processes still to be discovered] all play a part in understanding the paradox that was first pointed out over 150 years ago. Whatever the real answer is, one thing is certain, identification of the anomaly by Darwin has spurred others to delve deeply into coral reef ecology. And that has ultimately enriched our understanding of this important, but delicate and threatened, ecosystem. Trying to unravel Darwin’s Paradox is therefore one example of the many that underline the enduring relevance and importance of Darwin’s 19th century work as it continues to inform (plant) biology in the 21st century.
* Why are these coral reefs being described as warm-water? That’s because some coral reefs also exist in cold water. Because Darwin’s comments were based on his observations of reef-building corals in sunlight upper levels of the oceans in tropical regions – i.e. those found in warm water – warm-water is added for accuracy and clarification.
** Emphasising the continued fascination with Darwin’s Paradox, additional information regarding this phenomenon has also been provided in 2023. For example, Guoxin Cui et al. examined nitrogen recycling and transfer within the coral symbiosis in their publication entitled “Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia”. And Moyang Li et al. presented this study “Understanding nitrogen dynamics in coral holobionts: comprehensive review of processes, advancements, gaps, and future directions”.
*** However, whilst the focus of the research examined so far in this piece concentrates on a two-symbiont coral relationship, one wonders what role may be played by a so-called corallicolid, the name given to “a widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes” by Waldan Kwong et al.. This discovery that “coral symbiosis is a three-player game” (Thomas Richards & John McCutcheon) – involving coral polyp, photosynthetic alga, and an apicomplexan – potentially complicates our understanding of the movement of nutrients between the partners and arguably ‘opens up a whole new can of worms’. This revelation is rather reminiscent of the study of lichens by Toby Spribille et al. which reported the presence of “basidiomycete yeasts in the cortex of ascomycete macrolichens”. As for corals, that discovery also increased the number of partners in that mutually-beneficial symbiosis from two to three.
READ THE ARTICLES
Berendse, F. and Scheffer, M. (2009) “The angiosperm radiation revisited, an ecological explanation for Darwin’s ‘abominable mystery,’” Ecology Letters, 12(9), pp. 865–872. Available at: https://doi.org/10.1111/j.1461-0248.2009.01342.x.
de Boer, H.J., Eppinga, M.B., Wassen, M.J. and Dekker, S.C. (2012) “A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution,” Nature Communications, 3(1), pp. 1–11. Available at: https://doi.org/10.1038/ncomms2217.
Brandl, S.J., Tornabene, L., Goatley, C.H.R., Casey, J.M., Morais, R.A., Côté, I.M., Baldwin, C.C., Parravicini, V., Schiettekatte, N.M.D. and Bellwood, D.R. (2019) “Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning,” Science, 364(6446), pp. 1189–1192. Available at: https://doi.org/10.1126/science.aav3384.
Calvo Garzón, P. and Keijzer, F. (2011) “Plants: Adaptive behavior, root-brains, and minimal cognition,” Adaptive Behavior, 19(3), pp. 155–171. Available at: https://doi.org/10.1177/1059712311409446.
Calvo, P., Gagliano, M., Souza, G.M. and Trewavas, A. (2020) “Plants are intelligent, here’s how,” Annals of Botany, 125(1), pp. 11–28. Available at: https://doi.org/10.1093/aob/mcz155.
Castiello, U. (2023) “Plant intelligence from a comparative psychology perspective,” Biology, 12(6), p. 819. Available at: https://doi.org/10.3390/biology12060819.
Cui, G., Konciute, M.K., Ling, L., Esau, L., Raina, J.-B., Han, B., Salazar, O.R., Presnell, J.S., Rädecker, N., Zhong, H., Menzies, J., Cleves, P.A., Liew, Y.J., Krediet, C.J., Sawiccy, V., Cziesielski, M.J., Guagliardo, P., Bougoure, J., Pernice, M., Hirt, H., Voolstra, C.R., Weis, V.M., Pringle, J.R. and Aranda, M. (2023) “Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia,” Science Advances, 9(11). Available at: https://doi.org/10.1126/sciadv.adf7108.
Droxler, A.W. and Jorry, S.J. (2021) “The origin of modern atolls: Challenging Darwin’s deeply ingrained theory,” Annual Review of Marine Science, 13(1), pp. 537–573. Available at: https://doi.org/10.1146/annurev-marine-122414-034137.
Friedman, W.E. (2009) “The meaning of Darwin’s ‘abominable mystery,’” American Journal of Botany, 96(1), pp. 5–21. Available at: https://doi.org/10.3732/ajb.0800150.
Goatley, C.H.R. and Brandl, S.J. (2017) “Cryptobenthic reef fishes,” Current Biology, 27(11), pp. R452–R454. Available at: https://doi.org/10.1016/j.cub.2017.03.051.
de Goeij, J.M., van Oevelen, D., Vermeij, M.J.A., Osinga, R., Middelburg, J.J., de Goeij, A.F.P.M. and Admiraal, W. (2013) “Surviving in a marine desert: The sponge loop retains resources within coral reefs,” Science, 342(6154), pp. 108–110. Available at: https://doi.org/10.1126/science.1241981.
Gove, J.M., McManus, M.A., Neuheimer, A.B., Polovina, J.J., Drazen, J.C., Smith, C.R., Merrifield, M.A., Friedlander, A.M., Ehses, J.S., Young, C.W., Dillon, A.K. and Williams, G.J. (2016) “Near-island biological hotspots in barren ocean basins,” Nature Communications, 7(1), pp. 1–8. Available at: https://doi.org/10.1038/ncomms10581.
Gray, W.M. (2004) “Hormonal regulation of plant growth and development,” PLoS Biology, 2(9), p. e311. Available at: https://doi.org/10.1371/journal.pbio.0020311.
Khattar, J., Calvo, P., Vandebroek, I., Pandolfi, C. and Dahdouh-Guebas, F. (2022) “Understanding interdisciplinary perspectives of plant intelligence: Is it a matter of science, language, or subjectivity?,” Journal of Ethnobiology and Ethnomedicine, 18(1). Available at: https://doi.org/10.1186/s13002-022-00539-3.
Kwong, W.K., del Campo, J., Mathur, V., Vermeij, M.J.A. and Keeling, P.J. (2019) “A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes,” Nature, 568(7750), pp. 103–107. Available at: https://doi.org/10.1038/s41586-019-1072-z.
Li, M., Sheng, H.-X., Dai, M. and Kao, S.-J. (2023) “Understanding nitrogen dynamics in coral holobionts: comprehensive review of processes, advancements, gaps, and future directions,” Frontiers in Marine Science, 10. Available at: https://doi.org/10.3389/fmars.2023.1203399.
Micheneau, C., Johnson, S.D. and Fay, M.F. (2009) “Orchid pollination: from Darwin to the present day,” Botanical journal of the Linnean Society, 161(1), pp. 1–19. Available at: https://doi.org/10.1111/j.1095-8339.2009.00995.x.
Nagda, S. (2013) “How to write a scientific abstract,” Journal of Indian Prosthodontic Society. Available at: https://doi.org/10.1007/s13191-013-0299-x.
Richards, T.A. and McCutcheon, J.P. (2019) “Coral symbiosis is a three-player game,” Nature, 568(7750), pp. 41–42. Available at: https://doi.org/10.1038/d41586-019-00949-6.
Spribille, T., Tuovinen, V., Resl, P., Vanderpool, D., Wolinski, H., Aime, M.C., Schneider, K., Stabentheiner, E., Toome-Heller, M., Thor, G., Mayrhofer, H., Johannesson, H. and McCutcheon, J.P. (2016) “Basidiomycete yeasts in the cortex of ascomycete macrolichens,” Science, 353(6298), pp. 488–492. Available at: https://doi.org/10.1126/science.aaf8287.
Wiedenmann, J., D’Angelo, C., Mardones, M.L., Moore, S., Benkwitt, C.E., Graham, N.A.J., Hambach, B., Wilson, P.A., Vanstone, J., Eyal, G., Ben-Zvi, O., Loya, Y. and Genin, A. (2023) “Reef-building corals farm and feed on their photosynthetic symbionts,” Nature, 620(7976), pp. 1018–1024. Available at: https://doi.org/10.1038/s41586-023-06442-5.
Cover Image by Canva.