Desiccation tolerance

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Desiccation tolerance refers to the ability of an organism to withstand or endure extreme dryness, or drought-like conditions. Plants and animals living in arid or periodically arid environments such as temporary streams or ponds may face the challenge of desiccation, therefore physiological or behavioral adaptations to withstand these periods are necessary to ensure survival. In particular, insects occupy a wide range of ecologically diverse niches and, so, exhibit a variety of strategies to avoid desiccation.

Contents

In general, desiccation resistance in insects is measured by the change in mass during dry conditions. [1] The overall mass difference between measurements before and after aridity exposure is attributed to body water loss, as respiratory water loss is generally considered negligible.

Desiccation and plants

Desiccation tolerant plants include Craterostigma plantagineum , Lindernia brevidens and Ramonda serbica .

Desiccation sensitive plants include members of Arabidopsis genus, Lindernia subracemosa, Gossypium hirsutum , Triticum aestivum and Zea mays . [2]

Types of desiccation resistance

There are three main ways in which insects can increase their tolerance to desiccation: by increasing their total body water content; by reducing the rate of body water loss; and by tolerating a larger proportion of overall water loss from the body. [1] Survival time is determined by initial water content, and can be calculated by dividing water loss tolerance (the maximum amount of water that may be removed without resulting in death) by water loss rate. [1]

Increasing body water content

Insects with a higher initial body water content have better survival rates during arid conditions than insects with a lower initial body water content. [3] Higher amounts of internal body water lengthen the time necessary to remove the amount of water required to kill the organism. The way in which body water content is increased may differ depending on the species.

The accumulation of glycogen during the insect larval stage has been linked to increased body water content and is likely a source of metabolic water during dry conditions. [4] Glycogen, a glucose polysaccharide, acts as an oxidative energy source during times of physiological stress. Because it binds up to five times its weight in bulk water, insects with increased levels of body glycogen also have higher amounts of internal water. [3] In general, insects selected for desiccation resistance also exhibit longer larval stages than those sensitive to desiccation. [5] This increase in development time is likely a response to the environment, allowing larvae more time to accumulate glycogen, and therefore more water before eclosion.

Another possible source contributing to higher levels of initial body water in insects is hemolymph volume. The insect equivalent to blood, hemolymph is the fluid found within the hemocoel, and is the largest pool of extracellular water within the insect body. [6] In the fruit-fly Drosophila melanogaster , flies selected for desiccation resistance also yielded higher amounts of hemolymph. Higher hemolymph volume is linked to an increase in carbohydrates, in particular trehalose, a common sugar found in many plants and animals with high desiccation resistance. [6] Drosophila melanogaster flies selected for desiccation resistance show a 300% increase in hemolymph volume compared to control flies, correlating to a similar increase in trehalose levels. [6] During periods of aridity, cells dehydrate and draw upon hemolymph stores to replenish intracellular water; therefore, insects with higher levels of this fluid are less prone to desiccation.

Insects may also increase body water content by simply feeding more often. Because sugar is slowly absorbed into the hemolymph at each meal, increasing the frequency at which the insect ingests a sugar source also increases its desiccation tolerance. [3] Furthermore, the crop may also act not only to store food prior to digestion but to provide an additional reservoir for water and sugar. [3]

Reducing rate of water loss

Another strategy used to reduce the risk of death by dehydration is to reduce the rate at which water is lost. The three main ways through which insects can lose water are (1) the surface of the body (integument); (2) the tracheae (respiration); and (3) excretion, or waste products. [7] The important feature in reducing water loss in land snails during inactivity is an epiphragm. [8]

Integument

The exoskeleton or integument of insects acts as an impermeable, protective layer against desiccation. It is composed of an outer epicuticle, underlain by a procuticle that itself may be further divided into an exo- and endocuticle. [9] The endocuticle provides the insect with toughness and flexibility and the hard exocuticle serves to protect vulnerable body parts. However, the outer cuticular layer (epicuticle) is a protein-polyphenol complex made up of lipoproteins, fatty acids, and waxy molecules, and is the insect's primary defense against water loss. Many insect orders secrete an additional cement layer over their wax layer, likely to protect against the abrasion or removal of waxy molecules. This layer is composed of lipids and proteins held together by polyphenolic compounds and is secreted by the dermal glands.

In general, the rate of water loss in insects is low at moderate temperatures. Once a species-specific critical temperature (Tc) is reached, as temperatures continue to increase, rapid water loss occurs. The “lipid melting model” is used to explain this sudden increase in the rate of water loss. [10] The lipid melting model states that increased cuticular water loss is directly related to the melting of surface lipids. [10] Insects already adapted to more arid environments have a higher Tc; that is, their cuticular properties change and lipid structures melt at a higher critical temperature. [10]

In some insects, the rate of cuticular water loss is controlled to some extent by the neuroendocrine system. [11] Immediately following head removal, decapitated cockroaches exhibit a large increase in transpiration across the cuticle, leading to severe dehydration. Injection of brain hormones into freshly separated bodies results in a sharp reduction in cuticular water loss. [11]

Tracheae

In general, insects adapted to arid environments also have an impermeable cuticular membrane that prevents water loss. Therefore, a majority of water lost to the atmosphere occurs via the air-filled tracheae. [12] To help reduce water loss, many insects have outer coverings to their tracheae, or spiracles, which shut when open respiration is unnecessary and prevent water from escaping. Insects at a greater risk for water loss face the challenge of either a depleted oxygen supply or desiccation, leading to an adaptive increase in tracheal volume in order to receive more oxygen. [12]

Excretion

Following feeding, most insects retain enough water to completely hydrate their bodies, excreting the remainder. [13] However, the amount of water excreted differs between species, and depends on the relative humidity and dryness of the environment. For example, Tsetse flies maintained at a high relative humidity, and thus non-arid conditions, excrete fecal matter with approximately 75% water content, whereas Tsetse flies maintained at a low relative humidity, and thus dry conditions, excrete fecal matter with only 35% water content. [13] This adaptation helps minimize water loss in unfavorable conditions and increase chances of survival.

Tolerating greater water loss

Most insects can tolerate a 30-50% loss of body water; however, insects adapted to dry environments can tolerate a 40-60% loss of body water. [14] Initial body size also plays a large role in how much water loss can be tolerated, and, in general, larger insects can tolerate a larger percentage of body water loss than smaller insects. [15] The female beetle Alphitobius diaperinus, for example, is larger than its male counterpart and can thus tolerate 4% more water loss. It is hypothesized that larger insects have increased lipid reserves, preventing dehydration and desiccation. [15]

Behavior modification

In addition to physiological adaptations that increase desiccation resistance, behavioral responses of insects to arid environments significantly decrease dehydration potential. Drosophila melanogaster fruit flies, for example, will actively move to areas with higher atmospheric water content when placed in dry environments. [16] Also, the dung beetle buries food in underground chambers, thereby ensuring water and energy sources during periodically dry conditions. [17] Feeding location may also be altered to ensure body hydration. Some caterpillars preferentially feed on the underside of leaves, where microclimate has higher relative humidity. [18] In a highly time-consuming activity such as feeding, these insects significantly reduce their chances of desiccation.

Cryptobiosis (Anhydrobiosis)

Cryptobiosis refers to the state of an organism that has no detectable metabolic activity, resulting from extreme and unfavorable environmental conditions; anhydrobiosis refers to the state of surviving the loss of (almost) all body water. Although this state is commonly observed in invertebrates, only one insect is known to be cryptobiotic (anhydrobiotic), the African chironomid Polypedilum vanderplanki . Polypedilum vanderplanki undergoes anhydrobiosis, a cryptobiotic state wherein the body is completely dehydrated. The larvae of P. vanderplanki inhabit rock pools that commonly dry out completely. [19] In response, P. vanderplanki larvae enter an anhydrobiotic state, during which changes in body osmolarity trigger the production of large amounts of trehalose. Due to its capacity for water replacement and vitrification, the accumulation of trehalose prevents the death of the larvae from water loss. [19]

Related Research Articles

Hygroscopy is the phenomenon of attracting and holding water molecules via either absorption or adsorption from the surrounding environment, which is usually at normal or room temperature. If water molecules become suspended among the substance's molecules, adsorbing substances can become physically changed, e.g. changing in volume, boiling point, viscosity or some other physical characteristic or property of the substance. For example, a finely dispersed hygroscopic powder, such as a salt, may become clumpy over time due to collection of moisture from the surrounding environment.

<i>Drosophila melanogaster</i> Species of fruit fly

Drosophila melanogaster is a species of fly in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly", "pomace fly", or "banana fly". In the wild, D. melanogaster are attracted to rotting fruit and fermenting beverages, and are often found in orchards, kitchens and pubs.

<span class="mw-page-title-main">Hemolymph</span> Body fluid that circulates in the interior of an arthropod body

Hemolymph, or haemolymph, is a fluid, analogous to the blood in vertebrates, that circulates in the interior of the arthropod (invertebrate) body, remaining in direct contact with the animal's tissues. It is composed of a fluid plasma in which hemolymph cells called hemocytes are suspended. In addition to hemocytes, the plasma also contains many chemicals. It is the major tissue type of the open circulatory system characteristic of arthropods. In addition, some non-arthropods such as mollusks possess a hemolymphatic circulatory system.

<span class="mw-page-title-main">Desiccation</span> State of extreme dryness or process of thorough drying

Desiccation is the state of extreme dryness, or the process of extreme drying. A desiccant is a hygroscopic substance that induces or sustains such a state in its local vicinity in a moderately sealed container. The word desiccation comes from Latin de- 'thoroughly', and siccare 'to dry'.

<span class="mw-page-title-main">Diapause</span> Response delay in animal dormancy

In animal dormancy, diapause is the delay in development in response to regular and recurring periods of adverse environmental conditions. It is a physiological state with very specific initiating and inhibiting conditions. The mechanism is a means of surviving predictable, unfavorable environmental conditions, such as temperature extremes, drought, or reduced food availability. Diapause is observed in all the life stages of arthropods, especially insects.

Cold hardening is the physiological and biochemical process by which an organism prepares for cold weather.

<span class="mw-page-title-main">Cryptobiosis</span> Metabolic state of life

Cryptobiosis or anabiosis is a metabolic state in extremophilic organisms in response to adverse environmental conditions such as desiccation, freezing, and oxygen deficiency. In the cryptobiotic state, all measurable metabolic processes stop, preventing reproduction, development, and repair. When environmental conditions return to being hospitable, the organism will return to its metabolic state of life as it was prior to cryptobiosis.

<span class="mw-page-title-main">Desert ecology</span> The study of interactions between both biotic and abiotic components of desert environments

Desert ecology is the study of interactions between both biotic and abiotic components of desert environments. A desert ecosystem is defined by interactions between organisms, the climate in which they live, and any other non-living influences on the habitat. Deserts are arid regions that are generally associated with warm temperatures; however, cold deserts also exist. Deserts can be found in every continent, with the largest deserts located in Antarctica, the Arctic, Northern Africa, and the Middle East.

Enantiostasis is the ability of an open system, especially a living organism, to maintain and conserve its metabolic and physiological functions in response to variations in an unstable environment. Estuarine organisms typically undergo enantiostasis in order to survive with constantly changing salt concentrations. The Australian NSW Board of Studies defines the term in its Biology syllabus as "the maintenance of metabolic and physiological functions in response to variations in the environment".

<i>Selaginella lepidophylla</i> Species of spore-bearing plant

Selaginella lepidophylla, also known as a resurrection plant, is a species of desert plant in the spikemoss family (Selaginellaceae). It is native to the Chihuahuan Desert of the United States and Mexico. S. lepidophylla is renowned for its ability to survive almost complete desiccation. Resurrection plants are vascular rooted plants capable of surviving extreme desiccation, then resuming normal metabolic activity upon rehydration. The plant's hydro-responsive movements are governed by stem moisture content, tissue properties and a graded distribution of lignified cells affecting concentric stem stiffness and spiraling. During dry weather in its native habitat, its stems curl into a tight ball, uncurling only when exposed to moisture.

<i>Belgica antarctica</i> Species of fly

Belgica antarctica, the Antarctic midge, is a species of flightless midge, endemic to the continent of Antarctica. At 2–6 mm (0.08–0.2 in) long, it is the largest purely terrestrial animal native to the continent. It also has the smallest known insect genome as of 2014, with only 99 million base pairs of nucleotides and about 13500 genes. It is the only insect that can survive year-round in Antarctica.

<span class="mw-page-title-main">Insect winter ecology</span> Survival strategies of insects during winter

Insect winter ecology describes the overwinter survival strategies of insects, which are in many respects more similar to those of plants than to many other animals, such as mammals and birds. Unlike those animals, which can generate their own heat internally (endothermic), insects must rely on external sources to provide their heat (ectothermic). Thus, insects persisting in winter weather must tolerate freezing or rely on other mechanisms to avoid freezing. Loss of enzymatic function and eventual freezing due to low temperatures daily threatens the livelihood of these organisms during winter. Not surprisingly, insects have evolved a number of strategies to deal with the rigors of winter temperatures in places where they would otherwise not survive.

<i>Phyllomedusa sauvagii</i> Species of amphibian

Phyllomedusa sauvagii, the waxy monkey leaf frog or waxy monkey tree frog, is a species of frog in the subfamily Phyllomedusinae. It is native to South America, where it occurs in Argentina, Bolivia, Paraguay and Brazil. This species is arboreal, living in the vegetation of the Gran Chaco.

A xerophyte is a species of plant that has adaptations to survive in an environment with little liquid water. Examples of xerophytes include cacti, pineapple and some gymnosperm plants. The morphology and physiology of xerophytes are adapted to conserve water during dry periods. Some species called resurrection plants can survive long periods of extreme dryness or desiccation of their tissues, during which their metabolic activity may effectively shut down. Plants with such morphological and physiological adaptations are said to be xeromorphic. Xerophytes such as cacti are capable of withstanding extended periods of dry conditions as they have deep-spreading roots and capacity to store water. Their waxy, thorny leaves prevent loss of moisture.

Discontinuous gas-exchange cycles (DGC), also called discontinuous ventilation or discontinuous ventilatory cycles, follow one of several patterns of arthropod gas exchange that have been documented primarily in insects; they occur when the insect is at rest. During DGC, oxygen (O2) uptake and carbon dioxide (CO2) release from the whole insect follow a cyclical pattern characterized by periods of little to no release of CO2 to the external environment. Discontinuous gas exchange is traditionally defined in three phases, whose names reflect the behaviour of the spiracles: the closed phase, the flutter phase, and the open phase.

Polypedilum vanderplanki or the sleeping chironomid, is a dipteran in the family Chironomidae. It occurs in the semi-arid regions of the African continent. Its larvae are found in small tubular nests in the mud at the bottom of temporary pools that frequently dry out during the lifetime of P. vanderplanki larvae. Under these conditions, the larvae's body desiccates to as low as 3% water content by weight. In the dehydrated state the larvae become impervious to many extreme environmental conditions, and can survive temperatures from 3 K to up to 375 K, very high levels of gamma-rays, and exposure to vacuum. It is one of few metazoans that can withstand near complete desiccation (anhydrobiosis) in order to survive adverse environmental conditions. Slow desiccation enabled larvae to synthesize 38 μg trehalose/individual, and all of them recovered after rehydration, whereas larvae that were dehydrated 3 times faster accumulated only 6.8 μg trehalose/individual and none of them revived after rehydration. Late Embryo Abundant (LEA), anti-oxidant, and heat-shock proteins may also be involved in survival. This species is considered the most cold-tolerant insect species, able to survive liquid helium (−270 °C) exposure for up to 5 min. with a 100% survival rate when desiccated to 8% water content.

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Hemideina maori, also known as the mountain stone wētā, is a wētā of the family Anostostomatidae. They are a large, flightless, nocturnal orthopteran endemic to New Zealand. Mountain stone wētā are long lived and are found on many central mountain ranges in New Zealand's South Island.

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Tardigrade specific proteins are types of intrinsically disordered proteins specific to tardigrades. These proteins help tardigrades survive desiccation, one of the adaptations which contribute to tardigrade's extremotolerant nature. Tardigrade specific proteins are strongly influenced by their environment, leading to adaptive malleability across a variety of extreme abiotic environments.

References

  1. 1 2 3 Chown, S.L.; Nicolson, S.W. (2004). "Insect Physiological Ecology". New York: Oxford University Press.
  2. ↑ Yuki Nakamura and Yonghua Li-Beisson (Editors) ISBN 9783319259772, Springer , p. 185, at Google Books
  3. 1 2 3 4 Gray, E.M.; Bradley, T.J. (2005). "Physiology of desiccation resistance in Anopheles gambiae and Anopheles arabiensis". American Journal of Tropical Medicine and Hygiene. 73 (3): 553–559. doi: 10.4269/ajtmh.2005.73.553 . PMID   16172480.
  4. ↑ Graves, J. L.; Toolson, E. C.; Jeong, C.; Vu, L.N. & Rose, M.R. (1992). "Desiccation, flight, glycogen and postponed senescence in Drosophila melanogaster". Physiological Zoology. 65 (2): 268–286. doi:10.1086/physzool.65.2.30158253. S2CID   29889650.
  5. ↑ Gefen, E.; Marlon, A.J.; Gibbs, A.G. (2006). "Selection for desiccation resistance in adult Drosophila melanogaster affects larval development and metabolite accumulation". Journal of Experimental Biology. 209 (Pt 17): 3293–3300. doi: 10.1242/jeb.02397 . PMID   16916965.
  6. 1 2 3 Folk, D.G.; Han, C.; Bradley, T.J. (2001). "Water acquisition and partitioning in Drosophila melanogaster: effects of selection for desiccation-resistance". Journal of Experimental Biology. 204 (Pt 19): 3323–3331. doi:10.1242/jeb.204.19.3323. PMID   11606606.
  7. ↑ Mellanby, K. (1934). "The evaporation of water from insects". Journal of Experimental Biology. 10 (3): 317–333. doi:10.1111/j.1469-185x.1935.tb00487.x. S2CID   84993444.
  8. ↑ Machin J. 1968. The Permeability of the Epiphragm of Terrestrial Snails to Water Vapor. Biological Bulletin, Vol. 134, No. 1 (Feb., 1968), pp. 87-95
  9. ↑ Wigglesworth, V.B. (1984). "Insect Physiology". Chapman and Hall, NY.
  10. 1 2 3 Gibbs, A.G. (2002). "Lipid melting and cuticular permeability: new insights into an old problem". Journal of Insect Physiology. 48 (4): 391–400. Bibcode:2002JInsP..48..391G. doi:10.1016/S0022-1910(02)00059-8. PMID   12770088.
  11. 1 2 Treherne, J.E.; Willmer, P.G. (1975). "Hormonal control of integumentary water loss: evidence for a novel neuroendocrine system in an insect (Periplaneta americana)". Journal of Experimental Biology. 63 (1): 143–159. doi:10.1242/jeb.63.1.143. PMID   1159358.
  12. 1 2 Snyder, G.K.; Sheafor, B.; Scholnick, D.; Farrelly, C. (1995). "Gas Exchange in the Insect Tracheal System". Journal of Theoretical Biology. 172 (3): 199–207. Bibcode:1995JThBi.172..199S. doi:10.1006/jtbi.1995.0016. PMID   7715192.
  13. 1 2 Bursell, E. (1960). "Loss of water by excretion and defaecation in the Tsetse fly". Journal of Experimental Biology. 37 (4): 689–697. doi:10.1242/jeb.37.4.689.
  14. ↑ Willmer, P.; Stone, G.; Johnston, I.A. (2000). "Environmental physiology of animals". New York: Blackwell Publishing.
  15. 1 2 Renault, D.; Coray, Y. (2004). "Water loss of male and female Alphitobius diaperinus (Coleoptera: Tenebrionidae) maintained under dry conditions". European Journal of Entomology. 101 (3): 491–494. doi: 10.14411/eje.2004.069 .
  16. ↑ Prince, G.J.; Parsons, P.A. (1977). "Adaptive Behaviour of Drosophila Adults in Relation to Temperature and Humidity". Australian Journal of Zoology. 25 (2): 285–290. doi:10.1071/ZO9770285.
  17. ↑ Halffter, G.; Edmonds, W.D. (1982). The Nesting Behavior of Dung Beetles (Scarabaeinae): An Ecological and Evolutive Approach. Mexico City, Mexico: Instituto de Ecologia.
  18. ↑ Rowley, M.; Hanson, F. (2007). "Humidity detection and hygropreference behavior in larvae of the tobacco hornworm, Manduca sexta". Journal of Insect Science. 7 (39): 1–10. doi:10.1673/031.007.3901. PMC   2999434 . PMID   20302460.
  19. 1 2 Watanbe, M.; Kikawada, T.; Okuda, T. (2003). "Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki". Journal of Experimental Biology. 206 (Pt 13): 2281–2286. doi: 10.1242/jeb.00418 . PMID   12771176.
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