Suitability of Terrestrial Tardigrada for Bryophytic Habitats
by Taylor Lockwood
BIOL/WATR 361, Spring 2015
The phylum Tardigrada, also known as water bears, is a very unique phylum. Terrestrial tardigrades are commonly found in the thin film of water on mosses and liverworts and have traits that make them highly suited for these bryophytic habitats. They have specialized feeding structures, allowing them to ingest the contents of cells. Their mode of reproduction allows them to repopulate even when only a single individual is present. They also exhibit various types of dormant resting stages, allowing them to survive the sometimes hostile conditions in bryophytes.
Feeding. — Moss is more than just a shelter for tardigrades. Their home is also their source of food. Tardigrades are generally herbivorous and use their pair of stylets to puncture the walls of moss cells, then suck out the fluid contents with their muscular pharynx. Some species of tardigrades are particular about which species of moss they eat when given a choice. The family Grimmiaceae appears to be favored by tardigrades, with their cell walls easy for them to pierce and suck from. The tardigrade species Macrobiotus sapiens has smaller stylets, making it difficult, but not impossible, for them to pierce the cells from moss in the families Pottiaceae and Orthotrichaceae. They will only eat from those families if Grimmiaceae is not available (Schill et al., 2011).
Moss is not the only food in their diet, which often includes algae. Algae is not indiscriminately eaten either. The morphology of algae largely determines whether or not it will be eaten. Many have a gelatinous covering that could make it difficult for the tardigrade. Others, such as Micrasteria rotata, with a size of 200 µm, may be too large for a tardigrade’s mouth, and the cell wall too tough to pierce. Chlorella vulgaris, with a size of 6 µm, may be too small to be eaten. The ideal diameter of algae is greater than 10 µm, the size of blue-green algae (Schill et al., 2011).
Bryophytes are habitats to more than just tardigrades. They also house other organisms, such as nematodes, rotifers, algae, and bacteria. Some species of tardigrades are carnivorous, and consume other smaller organisms, including other smaller tardigrades. Carnivorous tardigrades still have a pair of stylets and a sucking pharynx; however they are used to suck the contents from animal cells. In some cases, larger species may even suck in and consume the entire organism (Nelson, 2002).
Reproduction. — Since groups of tardigrades are largely isolated from each other in their own mosses, sexual reproduction is not always a viable option. Nearly all tardigrade species undergo parthenogenesis, with one marine species recorded as being hermaphroditic (Bertolani, 2001). All members of the terrestrial species are female. Since tardigrades can be dispersed on bits of moss by wind, parthenogenesis allows a single adult to colonize a new location. Because their environment could become unfavorable at any time, tardigrades must also be able to reproduce quickly when conditions are good (Bertolani, 2001).
Egg laying is usually synchronized with molting. The eggs may be laid either in the shed cuticle or freely into the moss (Bertolani, 2001). The female spreads out where her eggs are laid, in case some places are a better environment for the eggs. The timing of egg hatching is also varied. This helps prevent the entire clutch from hatching during an unfavorable time (Guidetti et al., 2011).
Dormancy. — Tardigrades are aquatic creatures, and require at least a constant film of water surrounding them at all times to be active. Bryophytes, unlike the ocean or lakes, are not constantly saturated with water and occasionally dry out. To survive this dehydration, or other unfavorable environmental conditions, tardigrades enter into a dormant state. They have two main types of dormancy: diapause and cryptobiosis. Cryptobiosis is induced when the environment conditions are too unfavorable or extreme, such as dehydration. Diapause is part of tardigrade physiology and does not have to be caused by environmental conditions, although the environment does often have role in it. Diapause and cryptobiosis can occur at the same time, which increases their resistance to unfavorable conditions.
The diapause state is represented by the formation of a cyst. Encystment is more common in freshwater tardigrades living in permanent bodies of water, but also occurs in terrestrial tardigrades. Encystment allows tardigrades to survive dehydration but does not protect them from extreme temperatures (Nelson, 2002).
The cyst is made up of many layers of cuticle surrounding the tardigrade, similar to an onion. The cysts are opaque and oval shaped, and the morphology varies between species and even within species (Guidetti et al., 2011). It is formed by first losing the mouth-parts, similar to molting. Unlike molting, the cuticle is not shed. They contract themselves to reduce their body size and halt all movement. Then the extra cuticle layers are produced (Bertolani et al., 2004). The new cuticle layers differ from the old one, with a more simple structure and reduced or absent claws. The mouth and the cloaca are also sealed off (Guidetti et al., 2011). Encystment is costly, because not only does an animal have to produce these new cuticles, but it also must be able to survive without food for months. To aid in this, their metabolism is greatly reduced while in the cyst state.
Encystment is caused by both external and internal stimuli and is associated with predictable adverse conditions, such as seasonal dry periods. Cysts are formed before the environmental changes occur, but the external stimuli that initiate and end encystment are not fully understood. Temperature, low oxygen, adverse pH, and energy reserve depletion have all been related to diapause, but it is not known if they trigger diapause, or if they are just the environmental conditions that encystment is known to withstand (Bertolani et al., 2004).
Cryptobiosis, on the other hand, is directly caused by adverse conditions. There are three commonly accepted forms: anhydrobiosis, cryobiosis, and anoxybiosis. These are induced by dehydration, low temperatures, and low oxygen, respectively. A fourth, osmobiosis, induced by high salt concentrations, is suspected but not yet proven (Guidetti et al., 2011).
Cryptobiosis involves the formation into a tun, a dehydrated state. This tun can be formed during any age or stage of life. While in a tun, tardigrades will not even die of old age (Nelson, 2002). As with encystment, the tardigrade contracts itself to reduce body size. Their legs are drawn inwards, forming a cylindrical shape (Møbjerg et al., 2011). They reduce or even cease all metabolic processes and lose much of their body water. Growth and reproduction are also stopped in this state. Tardigrades remain in a tun formation until the environmental conditions that triggered it are over.
For terrestrial tardigrades living on bryophytes, anhydrobiosis is possibly the most important form of cryptobiosis. Moss undergoes periods of wet and dry, and the organisms living in it must be able to survive the lack of water. To help with survival, tardigrades synthesize trehalose and glycerol sugars to protect their membrane during desiccation (Nelson, 2002). The tun that tardigrades form reduces their body surface, slowing the evaporation rate of their internal moisture. Occasionally, some tardigrades will aggregate together, to further reduce the amount of body surface exposed, although there are only a few documented instances of aggregation in natural populations (Guidetti, et al., 2011). Tardigrades have been known to survive in an anhydrobiotic state for years.
Cryobiosis allows tardigrades to survive freezing and thawing from extremely low temperatures, helping them survive in polar regions, such as on lichens in Antarctica (Nelson, 2002). Tardigrades can withstand cooling rates of 3.4°C/min, up to 30°C/min, and extremely low temperatures. They can survive for years at -80°C, and have been known to survive temperatures as low as -196°C. However, tardigrades can be damaged if they spend too much time at too low of a temperature (Guidetti et al., 2011).
There is little data collected regarding the tardigrade’s ability to undergo anoxybiosis, although they are sensitive to changes in oxygen levels. Guidetti et al. (2011) said that there are a number of terrestrial tardigrade species able to survive for days in an anoxic environment, but there is only data for a single littoral species. That species was found able to survive up to six months in a low oxygen environment.
In addition to dormant states, tardigrades also have resting eggs that are resistant to unfavorable condition. In an anhydrobiotic state, these eggs have been found to be viable even after nine years. The resting eggs need a stimulus to hatch — dehydration followed by rehydration (Bertolani et al., 2004). The eggs can also withstand extreme low temperatures and physical and chemical extremes (Guidetti et al., 2011).
These different dormant strategies allow tardigrades to survive in moss. Moss dries out slowly, which gives tardigrades time to undergo anhydrobiosis. Since moss and lichen can be found in some extreme environments, such as the Arctic or Antarctic regions, tardigrades must be able to survive extreme temperatures as well, which they can thanks to cryobiosis.
Tardigrades are strange and unique creatures living on mats of moss or on lichen. While they have unique traits that make them successful for living in bryophytes, bryophytes also have characteristics that make them habitable to tardigrades. The shape of their structure allows for air spaces within the plant tissue, providing sufficient oxygen for diffusion. They resist rapid changes in temperature and moisture, and they are saturated with water in their cushion (Merrifield & Ingham, 1998).
Tardigrades consume the same substrate they live in, and their reproductive strategy requires only a single individual to colonize a new moss cushion. Even though tardigrades are aquatic animals, they have the ability to survive years without water, simply by shutting themselves down and reviving themselves when conditions improve. This trait even allows them to visit the hostile vacuum of space and survive, the only animal with this accomplishment. Tardigrada is a unique and resilient phylum, and much is still to be learned about them.
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