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Oceanogr. Mar. Biol. Ann, Rev., 1963, 1, pp. 301-340. Harold Barnes, Ed. Publ, George Allen and Unwin Ltd., London THE EFFECTS OF TEMPERATURE AND SALINITY ON MARINE AND BRACKISH WATER ANIMALS* I. TEMPERATURE 0. KINNE Biologische Anstalt Helgoland, Zentrale Hamburg-Altona This review attempts to outline our present knowledge about the effects of temperature and salinity on marine and brackish water animals. It is, in essence, an ecological approach that includes relevant physiological data but excludes purely biochemical or biophysical aspects. It covers the Inverte- brata and Pisces. The restricted space allotment makes it impossible to review all pertinent papers. The literature on the effects of temperature alone would easily fill a whole volume. Only the main problems that have been studied and some general trends and relationships that have become apparent are considered here and are documented on the basis of a few subjectively selected examples or by referring to previous reviews. Temperature and salinity are two of the most potent physical factors in the life of marine and brackish water organisms. They largely characterize the physico-chemical properties of a given body of water. It has become increasingly evident from numerous papers that both factors should be considered together. There exists a complex correlation between the biological effects of temperature and salinity, the ‘temperature-salinity relation’ (tst): temperature can modify the effects of salinity and change (enlarge, narrow, shift) the salinity range of an organism, and salinity can modify the effects of temperature accordingly (Kinne, 1956a, 1957a, b; see also Clark, 1935; Kinne, 1952b, 1953b, 1960; McLeese, 1956; Verwey, 1957; Smith, 1957, 1959; Fliigel, 1959; Costlow, Bookhout and Monroe, 1960; Dehnel, 1960; Todd and Dehnel, 1960). In Part I of this review I shall consider some effects of temperature under constant conditions of salinity or in situations in which the salinity factor appears to have little bearing. In Part II, I shall first consider some effects of the salinity factor under comparable conditions; finally, in the last section attention will be paid to the combined effects of temperature and salinity. Changes in temperature and salinity affect various * Dedicated to Professor A. Remane on his 65th birthday. Ep. Nore. It was intended to publish Professor Kinne’s article as a whole but the exhaustive treatment led to the suggestion that it be split into two parts, namely, I. Temperature, and If. Salinity and Temperature-salinity combinations, a suggestion to which Professor Kinne has agreed. Part IL will be published in Volume II of this series. 302 O. KINNE physical and chemical properties of sea water, for example, the absorption coefficients of dissolved gases, osmotic pressure, density, electrical conduc- tivity, viscosity, absorption of radiation, refractive index, transmission of sound, relative proportions of water polymers containing 1, 2 or 3 elementary 20 molecules (mono-, di-, trihydroles). Such concomitant changes in the physico-chemical properties of the water must be taken into account in any detailed analysis of the specific effects of temperature and salinity on biological systems. Organisms react to their total environment rather than to single factors. This makes it extremely difficult to describe and evaluate details of the complex relationships between an organism and its environment parti- cularly since it is virtually impossible to measure simultaneously al/ physical, chemical and biological aspects of the environment of an aquatic organism under ecological conditions. We have to compromise here by aiming at a restriction to factors which are assumed to be most effective and which are readily measurable and easy to control. However, such a restriction should not be carried too far. A monofactorial analysis may lead to conclusions that ate ecologically invalid; it should be replaced wherever possible by a bi-, tri- or polyfactorial approach, including, for example, temperature, salinity, oxygen and light. Innumerable papers have been published concerning the effects of temperature on marine and brackish water animals. Recent reviews on or including this subject have been written by Bullock (1955), Prosser (1955), Precht, Christophersen and Hensel (1955), Gunter (1957), Moore (1958), Remane and Schlieper (1958), Crisp (1959), Brett (1960), Prosser and Brown (1961), and with respect to adaptation in Crustacea by Kinne (1963a, b). For basic considerations concerning temperature relations of organisms, temperature-rate functions, their mathematical formulation, and the so- called temperature rules, Bélehradek (1935), Allee, Emerson, Park, Park and Schmidt (1949), Heilbrunn (1952), Andrewartha and Birch (1954), Precht, Christophersen and Hensel (1955), Hedgpeth (1957), F. H. Johnson (1957), and Prosser and Brown (1961), should be consulted. The temperature of the open oceans ranges from about —2° to +30°C, and that of sea and brackish water areas closer to the continents from about —3° to +43°C. These ranges are small in comparison with the temperature Tasre I Average surface temperatures (°C) of the oceans between parallels of latitude. After Sverdrup, Johnson and Fleming (1942). North | Attantic | Indian | Pacific | south | Attantic | tndian | Pacific latitude | Ocean Ocean | Ocean | latitude | Ocean Ocean | Ocean | 70°-60° 5-60 70°-60” | —1-30 | —1-50| —1-30 60 -50 8-66 5:74 | 60-50 1:76 1°63 5-00 50 ~40 13-16 9:99 | 50-40 8-68 8-67] 11-16 40-30 | 20-40 18-62 | 40-30 16-90 17-00 | 16-98 30 -20 24-16 26-14 23-38 | 30-20 21-20 22°53 21-53 20-10 | 25-81 27-23 | 26-42 | 20-10 23-16 | 25-85] 25-11 10-0 | 26-66 | 27-88 | 27-20 | 10-0 25-18 | 27-41 | 26-01 303 TEMPERATURE AND SALINITY C7r6E Buywa},y pur uosuyor ‘dnspsaag sayy) “snSny pue Aren3qeq ur samnyeraduiay Beran usanyag soouarayIp oy suosoudax sofues emaesodwiey, “(21 (, A “Y) PwOUE LOHEIPET oY} UT soBuvs BuIpuodsoxi09 pur (,¥ 4, ¥ “W) @pnaney isurese poyo]d suvaco quoTEIP oY) WI amNyeradtuay sowsins Jo SodueT fenuUL oFeIOAY—"T “Hy oe oe o Sh oe we oF oe NOD SanLtyy za é 0 : Ee > zp 2 2 to & Bae = NVA90 d1s1oVd ae 00 a oH z gr 08 “18 nee osm = e So a 2 8 zoe” . “to gS = a a NV390 dIsiwd Oy, £0 Q see a 2 NV300 NVIONI g oo © nO 2 5 a 38 2 4 ce m 5B 2 26 : mS 2 y 63 z 8g Nva90 O1LNV TLV s fa a 22 so $ NW390 OILNWILY = 304. ©. KINNE extremes observed on the continents which may be as low as —68-5°C (lowest recorded air temperature, Siberia, 1892) and as high as --65°C (+85°C in hot springs containing blue-green algac). The average surface temperatures of the oceans and the average annual ranges are shown in Table I and Figure 1 respectively. The annual Tanges of temperature, and often also the daily ones, are smallest in the tropics; both decrease with increasing depth. On the equator, water temperature is approximately 26°C at the surface, 13°C at 200m depths, 7-5°C at 400m, 4-5°C at 1,000 m, and 3-3°C at 2,000m (Ekman, 1953; see also Sverdrup, Johnson and Fleming, 1942; Fleming, 1957). Temperature is a measure of molecular agitation and thus largely determines the rate of chemical reactions and consequently the rate of metabolism and activity. With respect to life as a whole, temperature is presumably the most important single environmental entity. Aquatic invertebrates and fishes (poikilotherms) usually exhibit body temperatures that closely approximate those of the surrounding water; this is particularly true for representatives with low rates of metabolism and activity. However, the temperature of a metabolizing cell tends to be higher than that of its non-living environment because glycolysis and oxidation liberate heat. Body temperatures of large, active poikilotherms may therefore be above that of the water; it was found to be 0-012°C higher in trout (Halsband, 1953), 6°C higher in striped marlin (Morrow and Mauro, 1950), and up to 10°C higher in some rather active fresh-water fishes (Clausen, 1934). In spite of such exceptions, it appears safe to assume that aquatic inverte- brates and fishes are in general thermo-conformers and that water temperature decisively affects their rates of metabolism and activity. In considering the effects of temperature as an ecological factor, we have to pay attention not only to its absolute value but also to its pattern or dynamics, for example, a distinction has to be made between constant temperatures and fluctuating temperatures, between gradients, ranges, averages, frequency and intensity of changes, duration of a given pattern, and total summation. Within the same species the biological effects of a given temperature pattern may be different in different populations, at different ages, in different life cycle Stages or in the two sexes and may depend on the temperature history of the individual tested, as well as on present or past effects of other environmental factors. Up to this date most of the laboratory work has been done at constant temperatures. There is great need for experiments conducted under fluctuating temperature conditions. Many organisms encounter in their natural habitat temperature variations, and these may in some cases represent an important prerequisite for their well-being and the normal completion of their life cycle. A constant temperature of 20°C and temperatures fiuctuating between 15° and 25°C with an average of 20°C do not necessarily have the same biological effects. Thus the brackish water amphipod Gammarus duebeni exhibits normal rates of growth and reproduction, a normal sex ratio and life span only under temperature conditions simulating the annual fluctuations in the field (Kinne, 1952a, 1953a, b, c). On the other hand, many tropical species, cave dwellers, inhabitants of cold or hot springs, and especially of arctic and deep sea waters live in narrow limits of temperature; in abyssal or hadal waters, temperature is close to 4°C or within a few degrees of 0°C (for TEMPERATURE AND SALINITY 305 example, Bruun, 1957; Koczy, 1953). Some reef-building corals are confined to temperatures above 18° to 19°C, and all reef formation takes place between the surface minimal isotherm lines (isocrymes) of 20°C (Gunter, 1957; see also Wells, 1957). The lamellibranch Portlandia ( Yoldia) arctica usually lives in water below 4°C, and Pecten groenlandicus has never been found in water above 0°C (Jensen, 1942), TEMPERATURE AND FUNCTION TEMPERATURE TOLERANCE AND LETHAL TEMPERATURE In general, the total range of temperature tolerated in the state of active life is smallest in marine forms, larger in brackish and fresh-water forms and largest in terrestrial species. In the state of latent life, protoplasm has survived temperatures as low as about —270°C and as high as 150°C (Allee, Emerson, Park, Park and Schmidt, 1949). Active life of most marine and brackish water animals is restricted to temperatures between 0° and 35°C, although this range is usually much narrower for any given species. Organisms that can tolerate wide ranges of temperature are called eurytherm; those restricted to narrow ranges are called stenotherm. The latter may be either oligotherm (cold stenotherm) or polytherm (warm stenotherm). Such terms are useful to characterize large groups of organisms, even though they are of course relative in connotation. Typical eurytherm species appear to be less in number than stenotherm ones. Among marine and brackish water invertebrates and fishes the majority of the eurytherm species lives near the coast, especially in littoral arcas. Of these, sessile or hemisessile forms tend to be more eurytherm than vagil ones, and those with a cosmopolitan distribution are usually more eurytherm than stenotopic species. The majority of the stenotherm species lives in the open oceans. A small number of animals is capable of avoiding detrimental effects of extreme temperatures by forming more resistant, rather inactive, dormant stages such as cysts, winter eggs or menonts. Many animals avoid critical temperatures by vertical and horizontal migration into more suitable conditions. The temperature range tolerated is often more restricted during the sexual phase than during the asexual phase. In many species it is narrow during very early ontogenetic development, then increases somewhat and finally decreases again in the senile adult. Death from cold is as universal in marine and brackish water organisms as death from heat; it is particularly prevalent in warm-temperate and sub- tropical areas, which are subjected to cold periods irregularly (Brongersma- Sanders, 1957; Gunter, 1957), Examples of cold death in nature have been reported, for example, from Florida by Bangs (1895), Finch (1917), Storey and Gudger (1936) and Miller (1940), from the Bermuda Islands by Verrill (1901), from Danish waters by Blegvad (1929), Johansen (1929), Smidt (1944), and from the coast of Texas by Gunter and Hildebrand (1951) (in Bermuda and Texas temperatures did not fall below 7° and 4°C, respectively). Storey (1937) and Gunter (1957) claim that in Florida and Texas death of fishes and other animals during cold spells occurs at intervals of about 10 years. The lower limiting temperature is generally higher in warm water forms than in cold water ones. Thus among fishes of west Florida resistance to sudden cold spells is correlated with their distribution as temperate, 306 0. KINNE subtropical or tropical species (Storey, 1937). Fishes which spawn at high temperatures suffer heavier mortality during cold periods than do those with lower spawning temperatures (Johansen, 1929). Particularly in organisms with lower temperature limits above 0°C, a sudden fall in temperature seems to be more effective than the low temperature per se. According to Norman (1936), many fishes cannot survive a sudden temperature change of more than 6°C to 8°C, Gradual changes are tolerated much better; some species tolerate a gradual change of up to 30°C or 35°C. A number of marine and brackish water animals cannot withstand freezing conditions. In the Arctic, for example, populations of various intertidal forms, such as Littorina littorea suffer high mortality rates unless they avoid freezing by moving down below the low watermark when winter approaches (Blegvad, 1929). On a sandy beach in Denmark, two months of unusually severe freezing killed the total populations of the polychaete Scoloplos armiger and the molluscs Mytilus edulis, Scrobicularia plana and Littorina littorea; Arenicola marina suffered 95 per cent mortality, Cardium edule and Mya arenaria 80 per cent, Nereis diversicolor 70 per cent and Macoma baltica 33 per cent (Blegvad, 1929). In Danish offshore waters, high mortality of shallow-water species during “severe ice winters’ seems to be responsible for the fluctuations in abundance from year to year of invertebrate larvae (Thorson, 1946; p. 473). Similar reports on lethal effects of extreme low temperatures in the field have been published by Delphy (1917), Caullery (1929), Johansen (1929), Orton and Lewis (1931), and Smidt (1944). At the upper extreme, many organisms are killed by temperatures not far above those to which they are accustomed, for example, Semper (1881), Shelford (1916), Mayer (1914, 1918), Gowanloch and Hayes (1927), Henderson (1929), Newcombe, Miller and Chappell (1936), Broekhuysen (1940), Kinne (1954a). Animals from cold water may have an upper lethal temperature which lies below the lower lethal temperature of closely related species from warm water (Prosser and Brown, 1961). Limulus from Massachusetts died at 41°C, but specimens from Florida at 46-3°C. Aurelia from Halifax died at 26-8°C to 28°C, from Florida at 40°C (Mayer, 1914). A malacostracan from warm brackish waters of 37° to 47°C was moribund at 35°C, and its lower lethal temperature was as high as 30°C (Barkes, 1959) Among intertidal animals from different parts of the world, lethal temperature tends to increase as a function of height above low water level. In South Africa marine gastropods occupying the upper intertidal (longest exposure to high temperature) had an average lethal temperature of 43-0°C; the respective values in the lower levels were: 41-7°C in the mid-tidal, 39-5°C in the lower intertidal and 34-1°C in the sublittoral (Broekhuysen, 1940). An interesting aspect of the resistance to freezing is the fact that some organisms can tolerate body temperatures considerably below 0°C without freezing. In general, freezing-point determinations performed on marine and brackish-water animals have shown that the freezing point of body fiuids is similar to, or lower than that of the external medium. Exceptions are: estuarine and brine shrimps, semi-terrestrial crabs and teleosts. In salinities close to or above that of sea water these forms maintain hypo- osmotic body fluids, which would be expected to freeze at higher temperatures than sea water. Various circumstances, however, may suppress or delay freezing: (1) as is well known, aqueous solutions can supercool by several TEMPERATURE AND SALINITY 307 degrees particularly if contained in capillary spaces; (2) exposure to decreasing temperature leads first to extra cellular freezing, dehydration, and gelation, resulting in an increase in osmo-concentration of cell fluids and thus delaying freezing and augmenting cold resistance of cells; (3) bound water is more resistant to freezing than free water; (4) organic solvents with anti-freeze effect may be added to body fluids. Certain animals thus can withstand super- cooling well below the freezing point of water without internal ice formation. Arctic fish do not survive total freezing but may tolerate freezing of the body surface (Scholander, Flagg, Hock and Irving, 1953). In the deep fjords in Labrador, Canada, with water temperatures of about —1-7°C throughout the year, the freezing point of fishes has been found to be about —0-9°C. If these fish are ‘seeded’ with ice, they freeze immediately. In the shallower water, freezing points of —0-8°C were found in summer (water temperature: 5-0°C), and of —1-6°C in winter (water temperature: —1+5°C). The deep- water fish live in a state of permanent supercooling and in the blood of super- cooled fishes from the Hebron Fjord in Labrador, the presence of antifreeze substance(s) has been assumed to be responsible for facilitating such super- cooling (Scholander, van Dam, Kanwisher, Hammel and Gordon, 1957). Recent attempts to determine the chemical identity of such anti-freeze have given the following results: (2) the amount of anti-freeze added to the blood of shallow-water fishes is variable (the fishes examined in 1959 averaged only about 0-3° increase in serum freezing-point depression over summer values; the respective value found in 1956 by Scholander and his co-workers was about 0-7°C, (6) the extra blood concentration does not come from the common inorganic ions, glucose, glycerol, proteins or urea and ammonia; (c) the anti-freeze of thefjord cod, but not that of the sculpin, is probably a component of the non-protein nitrogen fraction (Gordon, Amdur and Scholander, 1959). An increase in blood osmo-concentration at low temperatures (winter) has been shown for several Crustacea, especially in salinities significantly below that of sea water, for example, in various aquatic and semi-terrestrial species (Widmann, 1935), Rhithropanopeus harrisii (Otto, 1934; Kinne and Rotthauwe, 1952), Eriocheir sinensis (Otto, 1937), Palaemonetes varians, Leander serratus (Panikkar, 1940b), Gammarus duebeni (Kinne, 1952b), Crangon crangon (Brockema, 1941; Fliigel, 1959). In supra-normal salinities, however, blood osmo-concentration may be lower at low temperatures than at high temperatures, for example, in Gammarus duebeni, and Rhithro- panopeus harrisii. In Nereis diversicolor no effect of temperature on blood ‘osmo-concentration could be demonstrated (Beadle, 1943). The phenomenon of supercooling is not confined to aquatic organisms: certain insects may be supercooled to as low as —40° to —50°C (Salt and Mail, 1943). Some frost- hardy insects use glycerol in high concentrations. as anti-freeze and super- cooling facilitator (Salt, 1956, 1959). The experimental determination of lethal temperatures provides a useful tool in assessing (1) inter- and intraspecific differences in temperature tolerance, (2) the physiological condition, (3) the status of acclimation to a given temperature (see Hathaway, 1927; Fry, Brett and Clawson, 1942; Fry; Hart and Walker, 1946; Fry, 1947, 1957a; Brett, 1956; McLeese, 1956). Tolerance to cold is much more variable and more difficult to measure than tolerance to heat. The marine shore fish Girella nigricans is killed by moderately low temperatures well above 0°C (Doudoroff, 1942). Certain invertebrates 308 O. KINNE such as rotifers, nematodes and tardigrades can, in a desiccated condition, survive several hours of exposure to temperatures as low as —272°C if cooled and warmed quickly to prevent the formation of ice crystals (Luyet and Gehenio, 1940; Gunter, 1957), A list of upper lethal temperatures for various marine molluscs has been compiled from data by Broekhuysen (1940) and Evans (1948) and published by Gunter (1957). A certain amount of dehydration and gelation tends to increase resistance to both cold and heat, see for example, Heilbrunn (1952), Christophersen and Precht (1953), Precht, Christophersen and Hensel (1955), Kinne (1953b, 1956a), Remane and Schlieper (1958). The causes of cold and heat death are complex and not well understood. Extreme low temperatures cause insufficient integration of nervous and metabolic processes, insufficient rates of energy liberation, changes in water and mineral balance and in the colloidal relations with water, such as forma- tion of ice crystals (disrupture of intracellular organization), increase in osmo-concentration resulting from extracellular freezing and followed by dehydration of cells, liquefaction of cortical protoplasm and gelation of the interior (for example, Bélehrédek, 1935, 1957; Heilbrunn, 1952; Precht, Christophersen and Hensel, 1955; Gunter, 1957; Prosser and Brown, 1961). Fatal effects of disrupture of protoplasmic organization by ice crystals have been reported for amoebae (Chambers and Hale, 1932) and plants (Levitt, 1958). Intertidal animals, however, may revive after cellular distortion by freezing. In intertidal invertebrates, especially molluscs, frozen at —15°C, only 55 to 65 per cent of the body water was actually frozen, Such freezing was accompanied by a rapid decline in oxygen consumption, which may have been the result of increased intercellular osmo-concentration rather than of the low ‘temperature per se (Kanwisher, 1955, 1957, 1959). Freezing upsets the pattern of water and salt distribution in the living organism. In a slowly freezing salt solution, water crystallizes and salt is concentrated and trapped in the interstices of such crystals, Osmo-concentration of the yet unfrozen fraction of the solution rises and, since initial freezing is usually extracellular, water is drawn out of the cells (Merryman, 1956). As freezing continues, bound water from ions or proteins freezes and the water balance becomes seriously disturbed. Extreme high temperatures tend to cause an insufficient supply of oxygen, failures in process integration, water loss by evaporation (desicca~ tion); enzymes pass the phase where inactivation exceeds activation and synthesis, lipids change in state, protoplasmic viscosity increases, and cell membranes become increasingly permeable; at still higher temperatures protein denaturation occurs and toxic substances may be released from damaged cells. METABOLISM AND ACTIVITY Within the frame set by the lower and upper lethal temperature, the functions of an organism may be subdivided into metabolism and activity (Fry, 1947). Metabolism is the total of all processes which use and convert material for maintenance, growth, reproduction and repair and which make the energy available whereby the organism continues to exist. Activity comprises such processes as breathing, swimming, fighting and courting; it is the result of the integrated metabolism: activity refers to what the organism does; how it behaves. In general, rates of metabolism and activity increase with increasing TEMPERATURE AND SALINITY 309 temperature over most of the temperature range tolerated and then often decrease suddenly near the upper lethal temperature (heat coma). The rates of increase are often different for different species, for different processes, and for different levels or ranges of temperature. In addition, rates are often significantly modified. by other factors such as salinity and oxygen. The use of Qio values as tools in physiology and ecology should therefore be con- sidered critically, especially with regard to complex phenomena such as metabolism and activity. For a number of Crustacean species Qi values for oxygen consumption have been found to range between 2-0 and 3-0, In the same individual Qyg values usually increase with decreasing temperature. TEMPERATURE -nePaooueTion +! <— crow ——_- 2 3 4 AGE ~¥R8, EGG-HATCH-EMERGE-NiGHATE - YEARLING ~ | GRILSE "— MATURING-ADULT-SPAWNING STAGE FAL WN 52 SU Fa, WN SP SU. FA. WN. SP SUL OFA. WM. SR SU. FA. WN. SEASON Fig. 2.—Schematic representation of thermal requirements for different life processes in Pacific salmon, compiled by reference to Donaldson and Foster 1941; Brett 1952; Brett and Alderdice 1958; Seymour 1956; Annual Reports of the International Pacific Salmon Fisheries Commission. (After Brett, 1960.) Individuals of different sizes may exhibit either a weight-dependent or a weight-independent Qj (Wolvekamp and Waterman, 1960). For detailed pertinent information on the effect of temperature on metabolism, recent reviews already referred to should be consulted. Numerous attempts have been made to express the relationship between temperature and velocity of biological processes mathematically. Various functions of an organism such as locomotion, growth and reproduction, may have somewhat different temperature ranges (p. 313). Knowledge of such ranges is of importance for the evaluation of the ecological potential of a species or population (Fig. 2). A detailed assessment necessitates Jong term rearing and breeding experiments in the laboratory under a varicty of conditions and parallel investigations in the field (Kinne, 1956b, 19576), and only a few such studies have been made. The effect of temperature on growth has been studied in some detail in various aquatic animals. 310 0. KINNE Examples are the lamellibranch Venus mercenaria (Loosanoft and Nomejko, 1951) and the fish Cyprinodon macularius (Fig. 3). In Cyprinodon growth from hatching to attainment of maturity is fastest at 30°C, and growth rates decrease in this order: 30°, 25°, 35°, 20°, 15°C. At 25°, 30° and 35°C, growth rate is very high in the first few weeks and then levels off. Maturity is reached first in 35° and 30°C. In 35°C growth rate decreases practically to zero 25 weeks after hatching. Growth continues longest at the lower temperature levels (15° and 20°C). At an age of about 8 to 10 weeks, the yo days, 20 £24 weeks poy Fig. 3.—Growth of the fish Cyprinodon macularius as a function of temperature at a salinity of 35%, and under conditions of restricted food supply. Each value represents the average total length of twelve individuals. All fish were born and raised under the given conditions. Abscissa: number of weeks or days after hatching. (After Kinne, 1960.) length superiority of the 25°, 30° and 35°C-series begins to decrease, and after about 35 weeks, the 20°C-fish reached the same size as the 35°C-fish. After 1 year, the 20°C-fish were of the same size as the 30°C-fish and after a still longer period they even surpassed these (Kinne, 1960). Thus the differences in growth rate established in young individuals do not necessarily persist in older ones. Initially slow-growing individuals may surpass initially fast-growing ones and ultimately reach a greater final length and age. In the majority of marine and brackish water invertebrates and fishes, growth appears to continue under normal conditions throughout most of their life. There is usually a marked retardation during the colder season and at the attainment of maturity. In some molluscs, such as Purpura Japillus, body growth is reported to occur only in immature specimens (Moore, 1938). In other animals body growth alternates with gonad growth (Moore, 1937), for example, in Echinus esculentus. Some corals grow at normal rates TEMPERATURE AND SALINITY 311 only in temperatures around 21°C (for example, Hesse, Allee and Schmidt, 1951; Hutchins and Scharff, 1947), For other pertinent examples on the effect of temperature on growth, see von Bertalanfly (1951), Brown (1957b), Moore (1958) and Waterman (1960). Since growth is correlated with size and shape, further reference to growth will be made in the section on temperature and structure (p. 324). ‘The capacity to osmo-regulate in salinities, hypo- or hyperosmotic to body fluids, may increase or decrease in various marine and brackish water animals as a function of temperature. A number of euryhaline crustaceans maintain their internal osmo-concentration more successfully near the lower end of their temperature range, when under hypo- or hyperosmotic stress. Examples ate the brachyurans Rhithropanopeus harrisii (Otto, 1934; Kinne and Rotthauwe, 1952), and Eriocheir sinensis (Otto, 1937), the amphipod Gainmarus duebeni (Kinne, 1952b), and the shrimp Crangon crangon (Fligel, 1959). In Crangon crangon Brockema (1941) originally reported that the osmo-regulative capacity was greater at high temperature (21°C) than at low temperature (4°C). Her results were obtained by measuring the electrical conductivity of the blood. They have been superseded by recent investi- gations (Fliigel, 1959), conducted at 5°, 10° and 15°C respectively, and employing the freezing-point technique. In general, the osmo-regulative capacity of a given species appears to be greatest at neat-optimum temperatures or somewhat below that (Kinne, 1952b, 1953b), and to decrease in supra- normal temperatures. Close to the lower or upper limits of the tolerated temperature range, osmo-regulation breaks down completely. Temperature affects not only the rate, but also the efficiency of metabolism. At the individual level, it affects the efficiency of conversion of food into body substance and into biologically useful energy. At the community level, it affects the rates and efficiencies of flow of material and energy, and hence may modify the species composition and dynamics of an eco-system. In her recent review on fishes, Brown (1957a) distinguishes between ‘gross efficiency’ and ‘net efficiency’. Gross efficiency represents the increase in body weight divided by the weight of food eaten. Net efficiency can be calculated by subtracting the weight of food required for maintenance from the weight of food eaten thus obtaining the weight of food available for growth, and then dividing the weight increase of the fish by this amount. In other words, ‘maintenance requirement’ is the amount of food which a fish must eat if it is neither to gain nor to lose weight; it provides for the routine metabolism, that is, basal metabolism plus normal activity (Brown, 1957a). Accurate measurements of maintenance requirements and net efficiency are difficult for several reasons: (1) maintenance requirements change with temperature and other environ- mental factors and with age (size) (for example, Dawes, 1930, 1931; Pentelow, 1939; Brown, 1946a, b); (2) fish are capable of adapting to different levels of feeding (for example, Brown, 1957a); (3) they are able to lower their standard metabolism during starvation (for example, Smith, 1955a, b; Phillips, 1954; Phillips and Brockway, 1954; Fry, 1957b). Maintenance requirements of plaice, Pleuronectes platessa, were less in winter than in summer and, when offered as much food as they would take (unrestricted food supply), plaice consumed much less in winter than in summer. Growth too was less in winter but the efficiency of food conversion was higher in winter than in summer (Dawes, 1931). In trout, Salmo trutta of equal sizes, maintenance requirements 312 ©. KINNE increased gradually at lower temperatures, rapidly at intermediate tempera- tures and again slowly at temperatures above 15°C (Brown, 1946). Brown interpreted these results as being due to variations of activity with temperature, suggesting that trout were most active between 10° and 12°C and that the decline in activity at higher temperatures (17° to 20°C) was sufficient to compensate for the expected increase in basal metabolism (Brown, 1946, 1957a). Gross efficiencies have been determined for Salmo trutta (Brown, 1957a), Cyprinodon macularius (Kinne, 1960), and some other fish. In the euryhaline desert pupfish, Cyprinodon macularius, gross efficiencies were determined in 35%, salinity at 5 different constant temperatures. Efficiencies obtained under restricted food supply conditions reach a maximum at 20°C, and in fish older than 12 weeks, decrease in the order: 20°, 15°, 25°, 30°, 35°C. Conversion efficiency decreases considerably under conditions of unrestricted food supply. In 140 day-old Cyprinodon macularius conversion was approximately half as efficient at 15°C as compared with the restricted supply, one-sixth as efficient at 30°C and about one-eighth as efficient at 35°C. In addition to temperature, conversion efficiency is affected by salinity, age, amount of water available per fish, quantity and quality of food offered, disturbances, light conditions, etc. At different levels of temperature, a given amount of food is converted by a given individual or population into different amounts of body substance and biologically useful energy. Simultaneously the rate of such transformation changes. Such alterations may significantly affect the dynamics and the species composition within an eco-system. Low efficiencies, for example, result in higher caloried faeces, and this in turn will tend to support organisms that are able to convert such material further (Kinne, 1960). In temperate seas most species have significantly reduced food require- ments during the cold months and often do not feed at all. In the Danish Macoma baltica community no growth and no predation seems to occur from late November to late April (Thorson, 1958). Such winter starvation has been reported also for the gastropods Urosalpinx cinerea (Galtsoff, Prytherch and Engle, 1937; Federighi, 1931; Hancock, 1954), Busycon carica and B. canaliculatum (Magelhaes, 1948), Ocenebra erinacea (Orton, 1929), Polinices heros and P. duplicata (Turner, 1950; Sawyer, 1950) and the fishes Pleuronectes platessa (Blegvad, 1917; Dawes, 1931) and Anguilla vulgaris (Blegvad, 1917). Plaice, Pleuronectes platessa from the North Sea area, which were normally growing and had to ‘hunt’ to find their food, ate 3 to 5 per cent of their own living weight of Mytilus flesh per day in the warm half-year. In the cold half-year they ate only one-tenth to one-twentieth of that amount, and below 0°C they stopped eating all together (Dawes, 1930, 1931; Biickmann, 1952). In spring and early summer, food requirements and growth rates increase drastically. At temperatures below 2°C, for example, growth practically ceases in the amphipod Gammarus duebeni, the isopod Sphaeroma hookeri and the mysid Neomysis integer, but it increases tre- mendously in spring as water temperatures rise (12° to 20°C) (Kinne, 1952c, 1954b, 1955). ‘Temperature may affect.a variety of physiological processes, for example, bioluminescence or phosphorescence (Gomazkov, 1958). It may also affect sex determination (for example, Kinne 1952a, 1953d, 1961; Lindsey, 1962), and, among other factors, it may act as a timer and provide reinforcements TEMPERATURE AND SALINITY 313 for rhythmical changes in metabolism and activity (Pearse, 1939; Gunter, 1957; Caspers, 1951; Korringa, 1957a; Pittendrigh, 1958; Brown, 1958, 1961, 1962). REPRODUCTION Of special importance are the effects of temperature on reproduction. In most animals reproductive processes are confined to narrower ranges than the majority of other functions. Thus the gastropod Urosalpinx cinerea requires higher temperatures for oviposition than for drilling or locomotion (Table ID), and the common American oyster, Crassostrea virginica, can feed TaBLe IL Minimum temperature requirements for oviposition, drilling and locomotion of the gastropod Urosalpinx cinerea. (After Stauber, 1950.) Activity Hampton Delaware Roads Race Bay Race Oviposition 20°C ee Drilling of oysters 15°C 10°C 10°C Sc and grow at much lower and higher temperatures than are required for spawning (Gunter, 1957). Rough approximations for Gammarus duebeni show that this brackish water amphipod can exist in North Germany in 10 per mille salinity at temperatures between 0° and 26°C while reproduction is possible only between 3° and 22°C (Kinne, 1953b, 1959), The respective values for existence and reproduction in three hydroids are: 2° and 20°C versus 7° and 19°C in Laomedea loveni; 2° and 24°C versus 12° and 19°C in Cordylophora caspia; 9° and more than 25°C versus 14° and 23°C in Peri- gonimus megas (Kinne, 1956c, d, €). It is necessary in such cases to distinguish between the vegetative temperature range and the reproductive temperature range. An animal with vegetative eurythermy and reproductive polysteno- thermy can make use of its eurythermic capacities only under certain conditions. It can occupy permanently cold waters only if it migrates to warmer waters for reproduction; it can occupy temporarily cold waters only if it succeeds in adjusting the timing of its reproductive period to the warm season. Conversely, a eurytherm animal with reproductive oligostenothermy would have to migrate into colder areas for reproduetion or adjust the timing of its reproduction to suitable temperatures during the cold season. On the basis of investigations by Runnstrém (1927) relationships between temperature and reproduction are demonstrated in Table ILI for Arctic-boreal boreal, and Mediterranean-boreal animals. Within the reproductive tempera- ture range it is often necessary to differentiate between temperature require- ments for maturation of sexual products, spawning and early development. Examples for differences in temperature ranges for ripening of gametes and 314 0. KINNE their release have been presented by Thorson (1946). Some lamellibranchs can be kept at temperatures high enough to induce gametogenesis but too low to permit spawning (Loosanoff and Davis, 1951). If such treatment is continued indefinitely, the oyster Crassostrea virginica finally reabsorbs its sexual products; in Venus mercenaria, however, gametes remain viable until the next season. Special temperature requirements during early development have become known, for example, from the European lobster, Homarus gammarus (syn.: H. vulgaris), whose larvae require temperatures above 15°C although the eggs, cleavage stages, and adults will tolerate lower temperatures (Appelldf, 1912). In most marine invertebrates, cleavage stages require narrower ranges of temperature than larval stages. TABLE TIT Spawning periods of some Arctie-boreal, boreal and Mediterranean-boreal animals at Bergen, Norway (Lat. 60° 25'N.). (After Runnstrém, 1927; from Sverdrup, Johnson, and Fleming, 1942.) ] | Fauna Animal gig \gld|aj2ia/s/dg|gig PERSP BP RR Aretic-boreal | Strongylocentrotus drobachiensis |x| x|x | | Cucumaria frondosa X|X/X Dendronotus frondosus x|x | Boreal Pleuronectes platessa x|x/|x Mytilus edulis x/x|x|x Echinus esculentus X|x|x| x] x Asterias rubens x[x x(x Mediterranean- | Psammechinus miliaris | x|x| x] x [> boreal Echinocvamus pusillus | x|x}x]x 1 Echinocardiwn flavescens | x}x}x)x/x] |] Echinocardiwn cordatum | x |x] x |x Ciona intestinalis | | [LE | = | | Once certain prerequisites are given, such as the appropriate physiological condition, food and space, the time of reproduction (breeding season) of most marine or brackish-water animals depends primarily on temperature. Other physical factors like salinity, light and pressure, or biological factors, are usually less important. While there may be a few species that breed all year round, most aquatic species begin to reproduce when a certain temperature level is reached, or in response to certain temperature changes. The idea introduced many years ago by Semper (1881) that tropical organisms have continuous breeding seasons requires qualification (Gunter, 1957). Yonge (1930) has shown that at the Great Barrier Reef many organisms have definite breeding rhythms; there are indications that the majority of tropical species spawn either exclusively or most actively in the warmer months (Stephenson, 1934), On the whole, the breeding seasons of tropical marine animals of a given community appear to be arranged so as to make the best use of time,