Coping with temperature extremes
Extreme temperatures are dangerous to many living systems. Proteins, including the enzymes that catalyze critical biochemical reactions, are temperature sensitive. High temperatures may cause structural degradation (denaturation),resulting in partial or complete loss of function. Death can come quickly to a seriously overheated animal. Cold temperatures can slow critical biochemical reactions by reducing molecular movement and interaction.
Living in water generally protects fishes from extreme environmental temperatures. Nevertheless, even at moderately high temperatures, fishes encounter an additional problem associated with the aquatic environment –decreased oxygen availability due to limited gas solubility. When combined with elevated oxygen demand due to increased metabolic rate and a temperature-induced Bohr effect that interferes with hemoglobin function, high temperatures result in a physiologically stressful situation (Gas transport). Not surprisingly, few fishes tolerate high temperatures (see Deserts and other seasonally arid habitats).
The physiological challenges of low temperature include compensating for the effects on cellular metabolism, nervous function, and cell membranes (Crockett &Londraville 2006). Probably the greatest potential danger at very low temperatures is intracellular formation of ice crystals which can puncture cell membranes and organelles, leading to cell death. Intracellular ice formation also causes extreme osmotic stress because as water freezes, solutes remain dissolved in a decreasing volume of cytoplasm, causing osmotic concentration to increase.
Freshwater fishes generally are protected from dangerously cold temperatures because fresh water freezes at 0°Cbut is densest at 4°C. Ice, therefore, forms on the surface of a lake or pond. Ions and other solutes depress the freezing point of the intracellular fluid of most fishes to around–0.7°C and freshwater fishes below the ice will not experience temperatures cold enough to freeze their body fluids. Freshwater fishes, therefore, seldom need special physiological mechanisms to cope with potentially freezing conditions.
Marine fishes at high latitudes, however, are faced with different circumstances (see Polar regions). Seawater freezes at about −1.86°C, which is below the freezing point of the body fluids of most fishes. A marine fish could, therefore, find itself in a situation where the temperature of its environment is lower than the fish’s freezing point – a potentially dangerous situation. Although some intertidal invertebrates and terrestrial vertebrates can survive freezing, fishes, instead, prevent ice formation through several different mechanisms.
One tactic involves a physical property of crystal formation. Crystals will not grow unless a “seed” crystal existsto which other molecules can adhere. Under controlled laboratory conditions, Mummichog (Fundulus heteroclitus)were cooled to about −3°C, well below their normal freezing point, without ice formation (Scholander et al. 1957),but when touched with ice crystals the fish froze nearly instantaneously. This phenomenon of supercoiling, also called undercooling, apparently is used by some marine fishes in very cold environments (Fletcher et al. 2001;DeVries& Cheng 2005). The potential danger of contacting ice crystals is less of a problem for fishes that live in deep water, where they are unlikely to encounter ice.
Many polar fishes do come in direct contact with ice, however, and still do not freeze, indicating that they have developed physiological mechanisms to prevent internal iceformation (DeVries & Cheng 2005; Adaptationsand constraints of Antarctic fishes). This protection generally involves the production of some type of biological antifreeze, a process which is controlled by genes that are activated seasonally (Fletcher et. al. 2001). Antifreeze compounds, usually proteins or glycoproteins, can bring the freezing point of some Antarctic fishes, particularly thenotothenioid ice fishes, down well below the freezing point of sea water (Fletcher et al. 2001; DeVreis & Cheng 2005).These antifreeze compounds are produced in the liver and distributed throughout the body, and they also are produced in tissues likely to contact ice, such as the skin, gills, and gut. Several different protein or glycoprotein antifreezes have been identified among cold water fishes, andall function by adhering to small ice crystals as they begin to form thereby preventing growth of the seed crystal.
The freezing point of body fluids also can be lowered by increasing the concentration of osmolytes (ions and other solutes) – the higher the concentration, the lower the freezing point. Notothenioids do this and achieve a slight (tenths of a degree) lowering of the freezing point. Other fishes rely strongly on increasing osmolytes to lower their freezing points in sea water. Rainbow Smelt (Osmeridae) use a combination of ice prevention tactics. They have an antifreeze in their blood to help prevent ice crystal growth. At very low temperatures, however, this antifreeze apparently is not enough protection, so the Rainbow Smelt produce glycerol to increase the osmotic concentration of the blood and intracellular fluids, thereby further decreasing the freezing point(Raymond 1992). At temperatures near the freezing point of sea water, the glycerol concentration is so high that the smelt are nearly isosmotic to the ocean. This increase in glycerol concentration is more apparent in the colder winter months and may account for the reported sweeter flavor of these fish during that time of year.
Other fishes that live in areas that have warmer and colder seasons, such as Atlantic Cod (Gadidae), ShorthornSculpin (Cottidae), and Winter Flounder (Pleuronectidae),also exhibit increased levels of biological antifreezes during winter (Fletcher et al. 2001). Because glycerol and protein or glycoprotein antifreezes are metabolically costly to produce, it makes sense to manufacture them only when needed; photoperiod seems to be the seasonal cue to increase or decrease antifreeze production (Fletcher et al.2001). Rainbow Smelt along the east coast of North America seem to rely mainly on the colligative properties of the glycerol to decrease the freezing point of their blood – they begin increasing levels of glycerol and antifreeze protein in their blood in fall, when water temperatures decline toabout 5°C (Lewis et al. 2004).
Species most likely to encounter ice have more copies of the genes that code for antifreeze production than fish that encounter less ice (Fletcher et al. 2001). Some have speculated that even within a species, higher latitude populationsmay be better equipped to deal with colder temperatures. However, although Atlantic Cod (Gadidae) from the northern tip of Newfoundland produced significantly more antifreeze glycoprotein than those from further south(Goddard et al. 1999), Purchase et al. (2001) showed that young cod raised from eggs and sperm from spawning adults captured in the Gulf of Maine (42°N, 70°W) were capable of producing as much antifreeze glycoprotein as young raised from spawning adults captured in the Grand Banks (46°N, 55°W) when both groups were exposed to equally low temperatures.
Very similar antifreeze compounds may occur in unrelated species, demonstrating convergent evolution at thegenetic and biochemical level. For example, northern cods (superorder Paracanthopterygii, family Gadidae) andAntarctic nototheniids (superorder Acanthopterygii, family Nototheniidae) have very similar antifreeze glycoproteins,but the genes responsible for producing them do not appear to be related. In another example, herring (subdivisionClupeomorpha, family Clupeidae), smelt (subdivision Euteleostei, superorder Protacanthopterygii, family Osmeridae,) and sea ravens (subdivision Euteleostei, superorderAcanthopterygii, family Cottidae) all have the same antifreeze protein. This is a different antifreeze, however, than is found in two sculpins, which are in the same family as the sea ravens. And each of these two sculpins (family Cottidae) have different antifreezes, suggesting that antifreeze compounds have evolved independently and perhapssomewhat recently in the Cottidae (Fletcher et al. 2001).
Antarctic fishes of the suborder Notothenioidei must maintain year-round protection from freezing because theirenvironment rarely gets above −1.5°C, even in summer. In most fishes molecules as small as glycoprotein antifreezes would be lost in the urine. The fish would then need to produce more, at considerable energetic cost. The urine of notothenioids, however, does not contain these antifreezes because the kidneys of these fishes lack glomeruli, the small clusters of capillaries through which blood normally is filtered(DeVries & Cheng 2005; kidney function, including glomerular kidneys).
Freeze protection strategies may not completely preventice formation within fishes. Small crystals of ice have beenfound in tissues that contact the surrounding water, such as the gills, skin, and gut. Ice also has been found in the spleen of some Antarctic fishes, perhaps carried there by macrophages that ingest small ice particles as part of the fish’s immune response (DeVries & Cheng 2005).