Rock Pools. We start with a small point, a small place in space and time, a rock pool. Perhaps you have seen a pool of water standing on a boulder after a summer rain. Most of us have seen puddles in roads after a downpour or standing in garden fountains. These ephemeral pools have a short life span, they may exist for a few hours or a few days, perhaps for a month and then they evaporate until the next rain. In drylands, the monsoon season delivers enough precipitation to create rock pools that last a month or more, but then the pools dry up and will not be seen again until the following year. In times of drought, the pools may not appear again for years.
Drought and desiccation. If you take the time to look, you will find that these pools are alive with a community adapted to the brief time span of ephemeral pools. Garden fountains host microbes, mosquitos, frogs, in some cases fish. Puddles in the middle of the road host fairy shrimp and tadpole shrimp. Rock pools support communities of biting and non-biting midges. Some of these species are just taking advantage of an available water resource, but others have their entire life cycle, their very lives dependent on the wax and wane of the temporary pool. They have very short life spans and must spend part of their life cycles in a stage that can exist in the absence of water, a stage that can resist or persist through desiccation.
Water bears and all. Some species survive months, years, even decades encysted in a protective covering that will allow them to resume development only in the presence of water. More rarely, some species survive desiccation in other developmental stages. The larvae of the African sleeping midge, Polypedilum vanderplanki Hinton 1951 go through the process of anhydrobiosis, a process through which they shrivel up and become inactive to survive long periods of heat and drought. These larvae were first described from rock pools in northern Nigeria and likely live in rockpools across the semi-arid regions of Africa, habitats that include periods of extensive drying and heat. Water bears or Tardigrades are relatively well known for the process of anhydrobiosis, but microbes, fungi, and some plants also survive drought this way. The African sleeping midge is notable because it is the largest animal that can go through complete desiccation via anhydrobiosis.
Sugar and glass. Amazingly, these larvae convert their tissues to a form of glass to survive the low water and high temperature conditions. First, their tissues accumulate high concentrations of a type of sugar called trehalose. These sugars then become glass via the process of vitrification. The result is a shriveled, small, vitreous individual that can remain in this state for long periods of time. Once the rains return to rehydrate the pools, the larvae convert back to their original forms and continue on to the rest of their life cycles: metamorphosis to the pupal stage followed by metamorphosis to the adult stage, mating, and laying eggs. One important aspect of their life cycles is that they may require a period of drying out or desiccation. In other words, they are so adapted to this strategy that they cannot live without it.
Ground control to major midge. Given the protection that vitrification provides, scientists began testing the environmental limits of these larvae, the point to which they can still survive, rehydrate, and continue on with their lives. Upper and lower temperature limits have been tested (-270°C to over 100°C). Length of time in the desiccated stage has been tested (at least 3 years). Tolerance to radiation has been tested (rehydration observed after doses as high as 3500 Gy). And finally, tolerance to the vacuum of space has been tested. Polypedilum vanderplanki survived 13 months in the vacuum of space in an experiment on the International Space Station, with 80% of the exposed larvae viably rehydrated.
Implications. It was not clear from the study whether the specimens exposed to space were viable after long periods of time or successfully reproduced, but they did survive these harsh conditions initially. As the largest animals exhibiting anhydrobiosis, they make excellent candidates for long term space voyages. They can serve as part of hydroponic ecosystems, a food source for humans, or a food source for any fish. We will not be keeping them out in the vacuum of space for these purposes, but their ability to withstand high radiation and temperature extremes in their shriveled up, glass-like state will provide an extra buffer should specimens ever be exposed to these conditions. Then they simply need be rehydrated and added to the environment to play their role in human exploration and colonization of space.
An afterthought. I am fascinated by the idea that these midges may be part of space exploration in the decades to come, but I am more excited by the role they play on Earth. My imagination was first captured by the discovery of tadpole shrimp jumping in a pool in the middle of a road in Colorado. Later I discovered midges living in muddy pools in Panama, observed fairy shrimp in road puddles in Mongolia as part of the MAIS research team, and found midges in garden fountains wherever I have lived. Some of the species in these habitats are uniquely adapted to the short life cycles and extreme conditions. They themselves are unique and are important parts of global and local biodiversity.
Further Reading
Crowe, J.H., Carpenter, J.F. and Crowe, L.M., 1998. The role of vitrification in anhydrobiosis. Annual review of physiology, 60(1), pp.73-103.
Hinton, H.E., 1951, August. A new Chironomid from Africa, the larva of which can be dehydrated without injury. In Proceedings of the Zoological Society of London (Vol. 121, No. 2, pp. 371-380). Oxford, UK: Blackwell Publishing Ltd.
Hinton, H.E., 1960. A Fly Larva that tolerates Dehydration and Temperatures of− 270° to+ 102° C. Nature, 188(4747), p.336.
Novikova, N., Gusev, O., Polikarpov, N., Deshevaya, E., Levinskikh, M., Alekseev, V., Okuda, T., Sugimoto, M., Sychev, V. and Grigoriev, А., 2011. Survival of dormant organisms after long-term exposure to the space environment. Acta Astronautica, 68(9-10), pp.1574-1580.
Sakurai, M., Furuki, T., Akao, K.I., Tanaka, D., Nakahara, Y., Kikawada, T., Watanabe, M. and Okuda, T., 2008. Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proceedings of the National Academy of Sciences, 105(13), pp.5093-5098.
Watanabe, M., Kikawada, T. and Okuda, T., 2003. Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. Journal of Experimental Biology, 206(13), pp.2281-2286.
Watanabe, M., Nakahara, Y., Sakashita, T., Kikawada, T., Fujita, A., Hamada, N., Horikawa, D.D., Wada, S., Kobayashi, Y. and Okuda, T., 2007. Physiological changes leading to anhydrobiosis improve radiation tolerance in Polypedilum vanderplanki larvae. Journal of insect physiology, 53(6), pp.573-579.
Wełnicz, W., Grohme, M.A., Kaczmarek, Ł., Schill, R.O. and Frohme, M., 2011. Anhydrobiosis in tardigrades—the last decade. Journal of insect physiology, 57(5), pp.577-583.
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