Dormancy Strategies in Tardigrades
by Crystal Buchholtz
BIOL/WATER 361, Fall 2013
For years, many have considered tardigrades to be among the hardiest animals known. They are able to survive anoxic conditions, exposure to radiation that would kill any human, conditions of no water, and even the vacuum of space. The word tardigrade is derived from the Latin word tardus meaning slow and gradu meaning step. They are bilaterally symmetrical eutelic organisms that are generally no larger than one millimeter in size and closely related to the arthropods. The common name for these animals, water bear, is given to them because of their microscopic bear-like appearance. However this is not what tardigrades are renowned for. They possess the miraculous ability to nearly shut down their all metabolic activity in their bodies at times of unfavorable conditions, stay that way for months, and “come back to life” when conditions once again become favorable. To do this, they must have various methods of dormancy. Tardigrades use a variety of dormancy strategies that can be broken down into diapause (encystment, cyclomorphosis, and resting eggs) and quiescence, or cryptobiosis (anhydrobiosis, osmobiosis, cryobiosis, and anoxybiosis). Although these processes differ in some ways, they all work towards the same goal: survival of unfavorable conditions through dormancy.
Although diapause and quiescence strategies achieve the same goal, they are different. Forms of quiescence are induced when environmental conditions become too extreme for the animal to handle, such as severe dehydration or lack of oxygen. This can happen at any point in the animal’s life cycle. Diapause, on the other hand, is a part of the animal’s physiology and development and does not necessarily have to be due to an environmental factor, although the environment plays a role many times.
Encystation is a diapause dormancy strategy utilized by many tardigrade species (common in freshwater tardigrades), and some species are only able to form cysts and not enter cryptobiosis. Bertolani et al. (2004) described encysted tardigrades as being made of multiple cuticles surrounding the organism in layers. To form the cyst, the animal appears to begin the molting process by shedding parts of the buccal-pharyngeal apparatus, but the old cuticle remains intact. The organism contracts its longitudinal muscles to reduce its body size and decreases body movements until the animal is completely still. Once the animal is still, two to three more cuticles are made. Depending on the species, the cuticle may be similar to that of a non-encysted tardigrade, or it may differ. Bertolani et al. (2004) briefly described two types of cysts: type 1 and type 2, the only significant difference being that the type 1 cyst generally has one less cuticle than type 2. Though these cysts are resistant to low amounts of water, they are not known to be able to resist extremely high temperatures (Nelson, 2002).
Recently, scientists have discovered that tardigrades are also taking part in cyclomorphosis, or the cyclic polymorphic conditions in response to changes in season, although not many species are known to do this. Halberg et al. (2009) recognized three stages of cyclomorphotic tardigrades: the active stage, the pseudosimplex 1 (P1), and the pseudosimplex 2 (P2). The active stage is present when conditions are favorable, such as spring and summer. The pseudosimplex 1 stage is known to occur during the winter (or another season depending on the location) when the sexually immature tardigrades hibernate. During the P1 stage, the tardigrade forms what is known as a movable cyst and this is the true hibernation period. During this stage, the animals are able to withstand freezing temperatures, however the longer they are exposed to subzero temperatures, the more likely it becomes that the animal will not survive (depending on the species). This means that the animals are able to tolerate internal ice formation in this stage. During the P1 stage, tardigrades aggregate. The development of gonads in the population seems to be synchronous, so that when the active stage is resumed, breeding can occur all at once. The P2 stage is not well observed in many tardigrade species, but is known to be a sexual maturation stage (Halberg et al., 2009).
The last diapause strategy of tardigrades is resting eggs. The first set of tardigrade eggs will hatch within 30-40 days and the delayed eggs typically hatch gradually between 41 and 62 days. Some eggs do not hatch in over 90 days. Of those eggs, some are resting eggs. In order for these eggs to hatch, they must be desiccated and rehydrated. These eggs will also become resting eggs when conditions are unfavorable for them to hatch. The eggs will wait until conditions become favorable, then they will hatch into juvenile tardigrades.
Quiescence (Cryptobiosis) Strategies
In all of the following dormancy strategies (except possibly anoxybiosis), tardigrades form what is called a tun. To form a tun, tardigrades will desiccate and draw in their legs and contract their body longitudinally, forming a barrel shape (Møbjerg et al., 2011). When in a tun, a tardigrade will nearly halt all metabolic activity and lose around 95 percent of the water in its body. The animal then produces a waxy substance for protection against total water loss. As the tardigrade continues to lose water, the tun shrinks and shrivels and reduces its surface area as much as possible. During tun formation, tardigrades have been known to accumulate a disaccharide called trehalose. It has been proposed that trehalose is used to replace the water that the animal loses during desiccation. Glycerol and heat shock proteins have also been found in desiccated tardigrades. It is believed that these assist in the recovery after the tun stage (Glime, 2013).
The cryptobiotic process of anhydrobiosis occurs when eggs, juveniles, or adult tardigrades are nearly completely dehydrated. During this stage, some species will withstand temperatures up to 70 degrees Celsius. Tardigrades undergoing anhydrobiosis will form a tun, and can be rehydrated to resume normal metabolic function. The slower the animal is dried, the more likely it is to survive the tun period (Glime, 2013).
Osmobiosis occurs when tardigrades are subjected to high osmotic pressures. Many tardigrades can withstand changes in salinity, but for those who cannot, they form a tun to protect themselves (Nelson, 2002). This only occurs when the salt concentration is higher on the outside of the outside of the organism’s body than the inside.
Cryobiosis is a form of cryptobiosis that differs from the others in that forming a tun is not always necessary. Cryobiosis is the result of very low temperatures and the water inside the tardigrade’s cells is in danger of freezing. To survive this, tardigrades have ice-nucleating proteins outside of their cells that draw the water out of the cells (Nelson, 2002). During cryobiosis, molecular movement comes to a stop. Unlike anhydrobiosis, cryobiosis can be rapid. This is observed in tardigrades that live near the Arctic and Antarctic.
Anoxybiosis is induced when there is a very low amount of oxygen in the habitat (Nelson, 2002). Not much is known about this state except the intake of water. Technically speaking, anoxybiosis is not a true form of cryptobiosis because the tardigrade does not form a tun in this state. In fact, instead of losing water, the animal will take in water. Lacking oxygen for too long will lead to the animal to lose control of osmoregularity, meaning more water than usual will rush into the cells. When this happens, the animal takes on a bloated-looking state and is immobile.
Example of Dormancy
Persson et al. (2011) discussed an experiment in which the space tolerance of tardigrades was tested. Tardigrades were sent into a low orbit around the earth and exposed to radiation and anoxic environments for a maximum of ten days. Before being exposed to this, the tardigrades were desiccated. Although low survival rates were observed in this experiment, some of the animals did survive. This shows the extreme stress tolerance of the tardigrades. If they can survive the vacuum of space for ten days, what else are these animals capable of?
The members of the phylum Tardigrada are truly remarkable organisms. Their two primary categories of dormancy, diapause and quiescence, or cryptobiosis, are characteristically different in how and when they occur. However, these dormancy strategies all work towards the same objective. They ensure the survival of the tardigrade where other animals would surely perish. There is yet much to be known about the dormancy strategies of tardigrades, but what we do know is that these animals are among the hardiest on this earth and much can be learned from them.
- Altiero, T., Bertolani, R. & Rebecchi, L. 2009. Hatching phenology and resting eggs in tardigrades. Journal of Zoology 280(3): 290-296.
- Bertolani, R., Guidetti, R., Jonsson, K.I., Altiero, T., Boschini, D. & Rebecchi, L. 2004. Experiences with dormancy in tardigrades. Journal of Limnology 63(1): 16-25.
- Glime, J.M. 2013. Tardigrade survival. Bryophyte Ecology, 2, Chapter 5.
- Halberg, K.A., Persson, D., Ramløv, H., Westh, P., Kristensen, R.M. & Mobjerg, N. 2009. Cyclomophosis in Tardigrada: adaption to environmental constraints. The Journal of Experimental Biology 212: 2803-2811.
- Nelson, D. & Marley, N. 2001. The biology and ecology of lotic Tardigrada. Freshwater Biology 44(1): 93-108.
- Nelson, D. 2002. Current status of the Tardigrada: evolution and ecology. Integrative and Comparative Biology 42(3): 652-659.
- Møbjerg, N., Halberg, K.A., Jørgensen, A., Persson, D., Bjørn, M., Ramløv, H. & Kristensen, R.M. 2011. Survival in extreme environments-on the current knowledge of adaptions in tardigrades. Acta Physiologica 202(3): 409-420.
- Persson, D., Halberg, K.A., Jørgensen, A., Ricci, C., Møbjerg, N. & Kristensen, R.M. 2011. Extreme stress tolerance in tardigrades: surviving space conditions in low earth orbit. Journal of Zoological Systematics and Evolutionary Research 49(1): 90-97.