Temperature

Temperature is a factor of prime importance in the marine environment because of its action (1) directly upon the physiological processes of the animals, especially upon the rate of metabolism and the reproductive cycle, and (2) indirectly through its influence on other environmental factors such as gases in solution, viscosity of the water, and density distribution with all its important hydrographic implications, discussed elsewhere.

An extensive literature has been built up pertaining to the effect of temperature on biological phenomena in the sea. This results first of all from the general recognition of the eminent importance of this factor and also from the fact that it is the most readily and accurately measured of the factors. This combination of circumstances may tend to give undue weight to the significance of temperature in relation to factors such as season, exchange or movement of water, and so forth, of which the temperature is only an index, and to factors such as density or viscosity which are functions of temperature (pp. 56 and 69). Nevertheless the abundant proof of its effects on life in the sea either directly or indirectly warrants a rather extensive review.

The range of temperature in the sea varies from about −3°C to 42°C, depending on season and locality, but in the open ocean the maximum temperature does not exceed 30°C. This range is small when

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contrasted with conditions in the air, where temperatures from −65°C to 65°C may be found.

It should be remembered, however, that in the cold-blooded or poikilothermic animals living in an aquatic environment all changes of temperature of the external medium are accompanied (because of the high conductivity of water) by an immediate change in the internal temperature of the body. The regulatory mechanisms developed in many terrestrial forms are wanting and vital processes must consequently be affected accordingly. It is therefore not surprising that within the narrow temperature range found in the sea there are temperature barriers segregating faunas into rather well-defined geographical regions of submarine climatic conditions that are controlled not only by latitude but also by depth of water and general circulation.

Animals are commonly divided into two large groups with reference to their tolerance to temperature range, namely stenothermic and eurythermic animals. But, as with other classifications, there are many intergradations between the typically stenothermic and the typically eurythermic forms and the degree of tolerance may also vary with the stage in the life history of the individual. Nevertheless, the classification is sufficiently distinctive to characterize vast numbers of species and therefore faunas in general.

Within the temperature limits tolerated by an animal there are three fundamental temperatures. These are the optimum, the maximum, and the minimum. The optimum temperature for any given species is not readily defined, since it is evidently not the same for all stages and functions of life, as is indicated in reproductive cycles associated with season. The maximum and minimum refer to the upper and lower limits of thermal tolerance. They also vary with the stage of the life cycle and the past thermal history of the individual. It is generally thought that the optimum temperature lies nearer the maximum than the minimum, but recent studies on fishes indicate that this is not always so (Doudoroff, 1942).

In areas with severe winters the intertidal animals are likely to be relatively few in number owing to winter destruction by freezing or to abrasion of beaches by ice. Wholesale destruction sometimes occurs in milder regions during unusually cold winter periods. In a special investigation on the mortality among intertidal animals of Danish waters during an unusually severe and protracted winter period in which ice formed on the beach and sand froze to a depth of 15 cm, Blegvad (1929) found a very marked destruction of animals. The percentage of animals killed in the area studied is as follows: Mytilus edulis, 100 per cent; Littorina litorea, 100 per cent; Cardium edule, 80 per cent; Nereis diversicolor, 70 per cent; Arenicola marina, 95 per cent; Mya arenaria, 80 per cent; Macoma baltica, 33 per cent.

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The optimum may be at the same or at a very different temperature for different species. Hence there are both cold-limited (phychrophile) and warmth-limited (thermophile) stenothermic forms, and as a result we find animals that are strictly endemic to cold- or warm-water areas of the ocean, as the case may be.

Geographic Distribution. It has been pointed out (Ekman, 1935) that early zoogeographers drew putative boundaries for littoral faunas based on climatic and hydrographic conditions. Rather little was known about the actual distribution limits of large numbers of species and faunal groups, but climatic boundaries had been discovered and the faunal areas were arranged according to these without their natural boundaries having been determined by empirical study. Zoogeographic boundaries must be determined in the final analysis by the actual distribution of the animals, but the marked importance of climate is shown by the fact that the early boundaries, drawn in the main speculatively, have been proved empirically to be well founded; which is to say that temperature is one of the most significant factors in the development of marine faunas.

Where temperature gradients are not well defined, the faunal zones do not have sharp boundaries either but merge one into the other with wide transition zones. The conditions in the Northeast Atlantic and the Northeast Pacific are considered especially illustrative of this. Along the east Atlantic coast, faunal boundaries are difficult to establish and a study of the isotherms of the North Atlantic reveals that the lines diverge toward the east and converge toward the west (charts II and III). For example, 36 per cent of the species of fishes found north of the Arctic Circle off Norway are found also in the Mediterranean. In the Northeast Pacific similar conditions are encountered, which are related to the divergence of isotherms on approaching the American continent. Here, however, the seasonal range in temperature is relatively small and upwelling along the coasts of North and South America keeps the coastal water cool to unusually low latitudes. The fauna of north temperate character has an extensive spread from the Bering Sea to Lower California, its closest affinities being with the Arctic rather than with the Tropical fauna. Among the arctic-temperate animals may be mentioned the genera Pandalus, Oregonia, Henricia. It must be noted also that in the east Atlantic boreal region the seasonal variations in water temperature are large in the coastal zone, having a range of 10° to 12°C off the coast of Norway and 10° to 15°C in the North Sea. These conditions tend to obliterate faunal boundaries for reasons discussed below.

Temperature and Reproduction. We have learned that there are many animals which are eurythermic while others are stenothermic, and that the stenothermic forms may be either warm stenothermic or cold stenothermic; that is, their optimum condition is at high or at low temperatures,

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respectively. This classification has been used mainly in reference to the adult animals, but a study of life cycles reveals that a closer analysis is necessary; for although some animals are either eurythermic or stenothermic throughout life, many others are eurythermic with respect to one phase of the life cycle and stenothermic at another phase. It is necessary therefore to distinguish between reproductive eurythermy or stenothermy during the spawning periods or during the egg or larval developmental stages, and the vegetative eurythermy or stenothermy during all other periods of life. It is well known that each species of animal usually has a more or less well-defined spawning season, especially in localities with marked seasonal changes. This periodicity appears to be correlated largely with temperature and the response may be to a change which results in a rising or falling temperature. In general, it may be said that the temperature limits are much more narrow for reproductive processes and for survival of eggs and young than for the older stages, wherefore the synchronizing of the spawning period with the proper season is essential. A vegetative eurythermic animal with reproductive stenothermy will usually be limited in its distribution to areas climatically suited to its propagative period and to its stenothermic young. This is not so restrictive as it at first appears, but it does involve a seasonal adjustment of spawning time to suit the requirements. Thus, if spawning and the resultant young require warmth, the summer season becomes the reproductive season, and winter-spawning animals of lower latitudes can live in boreal waters only by adjusting their spawning to the summer months in the north. Conversely, northern forms with stenothermic young may spawn in the north during summer and in the south during winter.

The very mixed fauna of the European boreal region is believed to be accounted for partly by these adjustments to suitable spawning season, for in these waters the seasonal range of temperature is sufficient to allow for northern and southern vegetative eurythermic forms to find periods suitable for stenothermic reproduction in the same area.

Results of examination of different species of oysters illustrate the variations in the critical spawning temperatures of marine animals. For both economic and scientific reasons, these animals have been studied in great detail by Trevor Kincaid, W. R. Coe, and others mentioned below, and the following minimum spawning temperatures have been established with considerable certainty (review by Hopkins, 1937):

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Although the above temperatures may be considered threshold temperatures, they can operate as determining factors only when other external and internal conditions are also within the favorable range. For example, the gonads must have reached the proper degree of development, which is itself a function of temperature and nourishment; the pH must be favorable, about 8.2 for Ostrea virginica (Prytherch, 1929); the presence of spermatozoa in the water may be necessary; and other uncertain factors also are involved (Galtsoff, 1930, 1938). The temperatures given above represent findings relative to the initiation of female spawning. Once begun it may continue at higher temperatures.

A good deal of evidence, both observational and experimental, shows that the distribution of many marine animals is dependent upon the above type of adjustments of critical reproductive periods within rather narrow temperature ranges. Orton (1920) concluded that:

A review of all the information collected bearing on the influence of temperature changes on breeding leads one to the conclusion that a temperature stimulus of some kind is the normal impulse for inducing sexual activity in marine animals assuming normal biological conditions. In marine invertebrates, at least, the impression is gathered that normal salinity variations within the habitat of the species have little effect on breeding. Since temperature is known to be of paramount importance in controlling distribution, it would seem that its influence on breeding is one of the ways in which the controlling effect is exerted.

Figure 234 and table 98, from an investigation by Runnström (1927), will serve to illustrate the relation between temperature and reproduction and larval survival of littoral marine fauna, of Arctic-boreal, boreal, and Mediterranean-boreal types of animals in boreal waters.

Vegetative distribution, especially of pelagic forms, may extend to areas beyond the limits set by the reproductive stenothermy; but such areas must be restocked regularly by adults or juveniles drifting in from favorable outside areas. This extended distribution is known as sterile distribution, and though the failure to reproduce in these extended areas may result from external environmental factors other than temperature, temperature seems nevertheless to be the major cause. It has been found, for instance, in the Bay of Fundy, that some species of fishes with floating eggs and such forms as the medusa Aglantha, the amphipod Parathemisto, the arrow worm Sagitta elegans, and still other forms either fail to reproduce at all or have very restricted success in reproduction although spawnings may occur (Huntsman and Reid, 1921, Fish and Johnson, 1937). The bulk of these animals must therefore be recruited seasonally by means of waters flowing in from the Gulf of Maine.

In the Gulf of Maine, Bigelow (1926) found that Sagitta serratodentata is a common constituent of the plankton. It thrives in these waters in the juvenile and adult stages, growing to a size greater than in its normal breeding habitat, but it is unable to breed in the Gulf because of the cold water. In the inner parts of the Gulf it succumbs during the winter and must be replenished each year by a new supply coming in with mixed water from the neighboring Gulf Stream. Its normal distribution is in waters above about 15°C.

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The tropical and subtropical copepod Eucalanus elongatus is carried far north with the Gulf Stream, but only adult or submature specimens appear to survive in the gradually cooling waters approaching the higher latitudes (Farran, 1911, With, 1915).

One of the most striking instances of the effectiveness of temperature differences as a barrier to distribution of benthic animals in the open deep sea is shown by a study of the fauna on the two sides of the Wyville Thomson Ridge (Murray and Hjort, 1912). Over this ridge, covered by water to a depth of about 500 m and connecting the Shetland and Faeroe Islands, the Gulf Stream water flows into the cold Norwegian Sea (p. 652). At the top of the ridge temperatures on both sides are only moderately different, but bottom temperatures of 4°C are found at a depth of 1500 m on the south or Atlantic slope while on the northern slope in the Norwegian Sea the temperature is 4°C at about 600 m, 0°C at 850 m, and −0.41°C in the bottom waters. An analysis of the fauna of each side showed that only 48 species and varieties, or about 11 per cent of a total of 433 enumerated by Murray, are common to both sides.

Bipolarity. It has long been known that the faunas of the cold waters of the north and south latitudes contain many elements in common. The animals or animal groups that form these elements may be wanting in the intervening tropical region. A break in the continuity of distribution of a species or higher division is called discontinuous distribution; when it occurs in a meridional direction so that the animals involved are absent from the tropical belt, the phenomenon is known as bipolar distribution or bipolarity. According to the older concept, only the arctic and antarctic regions are involved, but more recent usage includes the temperate zones also, and bipolar animals need not necessarily be polar. This is bipolarity of relationship and may be defined as a bipolar distribution in which animals of higher latitudes are more closely related taxonomically to each other than to those of lower latitudes. There is also bipolarity of phenomena such as are associated with mass vernal production of diatoms, for example, or with production of great numbers of individuals but of relatively few species.

Associated with bipolarity of relationship is the phenomenon of tropical submergence. Stenothermic animals that require cold water can of course find this by seeking greater depths; if they are sufficiently euryhaline and eurybathic, northern littoral or surface pelagic animals may form a continuous distribution from high northern to high southern latitudes by living in deep water in that part of their meridional range

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crossing the equatorial region. This tropical submergence has explained many instances of what was formerly believed to be bipolar distribution until the animals were discovered inhabiting also the cold deep waters of the intervening tropics. Great caution must accordingly be exercised when trying to establish groups of bipolar animals. Recently the term bipolar-epiplanktonic has been proposed (Russell, 1935b) to describe the distribution of related high northern and high southern planktonic animals connected through equatorial submergence, being mesoplanktonic in the warm latitudes. Six copepod species and other holoplanktonic animals make a total of 17 species from several groups that are included under this classification.

Examples of bipolarity are found in the gephyrean Priapulus caudatus of the Northern Hemisphere and a subspecies in the Southern Hemisphere. The pteropods Limacina helicina and Clione limacina of the north have related forms in the Southern Hemisphere. Other examples are the ascidian Didemnum albidum, and the shark Lamna cornubica. Bipolarity is not confined to species; the counterparts may be genera or families, in which cases bipolarity seems to be of older standing.

Since we are interested here mainly in showing the influence of temperature on distribution as illustrated by bipolarity, it is not proposed to discuss fully the means by which bipolarity was established. Two chief hypotheses have been advanced, the first holding that bipolar animals are relics of a previously cosmopolitan fauna, the tropical portion of which is now extinct; the second hypothesis holds that animals have migrated through cold deep water. A third hypothesis involves parallel development of the bipolar forms. It has been pointed out that the first two hypotheses do not conflict but are only different interpretations of the same idea, which we must accept under any circumstances if we consider the subject from the viewpoint of the history of development, to wit, that today's discontinuity emerged from yesterday's continuity. For one species the discontinuous distribution may have developed according to one hypothesis and for another species according to another; therefore each case must be studied independently.

Recently, through the purposeful efforts of man, a bipolarity has apparently been established in the Pacific salmon Oncorhynchus. The native distribution of this fish is confined mainly to the temperate waters of the North Pacific, but extends also into colder waters of the adjacent northern seas. Foreign transplantation of species of this genus has been successful in South Island, New Zealand, and at the southern tip of Chile. Many attempts to establish these migratory fish in the intervening areas of the tropical region between the native range and the new locations have met with failure. A study of the limiting environmental factors (Davidson and Hutchinson, 1938) shows that the temperature conditions at the newly established localities are comparable to those at the southern

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range of distribution of the species in the native North Pacific habitat. Since these fish are anadromous, both the marine and stream conditions must be suitable to complete all phases of the life cycle.

The effect of temperature differences on animals influences the vertical as well as the horizontal distribution. This was illustrated by the tropical submergence of forms which, showing a continuous meridional distribution, inhabit both high southern and high northern latitudes.

In arctic waters, where the range of temperature between deep and shallow water is small compared with differences between shallow and deep water of lower latitudes, the demarcations between littoral and deep-water fauna are less clearly defined. Examples of this are the sea star Hymenaster pellucidus and the pycnogonid Nymphon robustum, each of which occurs in the Norwegian Sea at depths of 2000 m, while near Spitsbergen the former occurs at 27 m and the latter thrives at 6 m. It appears from these and many other instances that temperature and not depth is the controlling factor. In a study of recent foraminifera in ocean sediments extending from lagoonal conditions to a depth of 2540 m, Natland (1933) found that the vertical distribution of the animals was arranged in five zones, each with certain key species correlated with submarine temperatures. A complementary study showed the same type of zonation of the same species in fossil-bearing geological strata of outcrops and oil-well borings in the same general region, thus providing a means of arriving at the probable temperature and perhaps, therefore, also the depth of water and other conditions that prevailed when these strata were formed as sediments on the bottom of the sea. In other words, this zonation is illustrative of the fact that dissimilar fossil faunas may have been contemporaneous but may also have lived under different environmental conditions with respect to temperature.

Pelagic animals also show a degree of bathymetric stratification which may be associated with the temperature distribution in the sea. In this connection it is difficult, however, to isolate the effect of temperature from that of light or to find out whether the temperature exercises a direct or an indirect influence. Indirectly it may act through its influence on viscosity, or it may change the reactions of the animals to gravity or to light, that is, change the sign of tropism with respect to these factors. Even in the phenomenon of tropical submergence we must not fail to be aware of the fact that light, owing to the great intensity of the tropical sun, may possibly force some animals, especially pelagic animals, to seek greater depths.

In the discussion of diurnal migrations we noted that the sharp temperature gradient frequently encountered at the thermocline deters some of the deeper migrants from coming to the surface or some of those living normally near the surface from venturing below into markedly colder water (p. 838). Bigelow and Sears (1939) indicate that, aside from

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diurnal migrations, the vertical distribution of boreal plankton of the continental shelf south of Cape Cod is subject to thermal control when summer surface temperatures rise above 14°C. The population, when consisting largely of Calanus finmarchicus, had its greatest density in water of 6° to 10°C.

Species of the fish genus Cyclothone descend to greater depths in southern than in northern waters. Among crustaceans the larger individuals of the pelagic prawn Acanthephyra purpurea occur at a depth of 500 to 750 m in the northern section traversed by the Michael Sars. In the lower latitudes these were found most abundant at 1000 m.

Metabolism. The optimum temperature for life activity is considered to be nearer the maximum than the minimum limit, for which reason a small rise in temperature from the optimum is more likely to be disastrous to cold-blooded animals than is a greater lowering (see p. 844). The latter will result in a marked slowing up of vital processes, but if not extreme may actually lead to an extension of the individual's life by inducing a period of quiescence when other factors, especially food supply, are at a minimum. This life extension may be illustrated by such forms as Calanus finmarchicus and C. hyperboreus, which during the winter months sink to, or seek, deeper water (200 to 300 m in some areas) and reduce their migratory activities (Gran, 1902, Sömme, 1934). Experimental tests have also indicated that Calanus grows and moults into successively older stages less rapidly at a temperature of 3°C than at temperatures of 6°C and 9°C, but survival is definitely better at the lowest temperature (Clarke and Bonnet, 1939).

The rate of metabolism (measured by oxygen consumption and production of carbon dioxide) of all poikilothermic organisms is very much increased with rise of temperature. According to van't Hoff's rule the increase is two to three times for each 10°C rise in temperature within favorable limits. Hence, it serves as one of the factors in the rapid and abundant spring production in boreal regions. During the winter when food supply is at a minimum in boreal waters, Calanus finmarchicus, for example, in copepodid stage V is found to sink to deep water, as already mentioned, where the temperatures are uniformly low and metabolism is accordingly slowed up. Here the animals may remain more or less quiescent until the return of spring, when they approach the surface, assume the adult state, and spawn in the upper water layers at a time when food has again become abundant. Among the coastal forms, the daphnids Podon and Evadne survive the low winter temperatures as resistant resting eggs. Rotifers and perhaps other coastal animals may do likewise, and are therefore able to appear suddenly in abundance in the spring plankton when vernal warming has taken place.

Numerous experiments have shown that oxygen consumption increases directly with rise in temperature. For a typical planktonic animal,

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Calanus finmarchicus, Marshall, Nicholls, and Orr (1935) found that oxygen consumption is about one half greater at 10°C than at 0°C, but at 20°C it is more than twice that at 10°C. Thus the effect of temperature increase on rate of metabolism is not the same throughout the range although the trend is always upward within tolerable limits. For females of adult Stage VI the oxygen consumed per hour by 1000 individuals varied with the temperature as follows: 0°C, 0.28 ml/hr; 5°C, 0.31 ml/hr; 10°C, 0.40 ml/hr; 15°C, 0.57 ml/hr; 20°C, 0.83 ml/hr. Stage V specimens showed less consumption throughout the range (the lowest corresponding value being 0.13 ml/hr and the highest 0.61 ml/hr) and it is of interest to note that the species spend the winter mainly in Stage V. The lower rate of metabolism of this stage should enable the animals better to survive the winter period when plankton food is scarce.

Calcium Precipitation. Temperature influences to a marked degree the rate at which calcium carbonate can be precipitated by animals in the formation of skeletal parts, shells, and spicules. The chemical reactions involved are not clearly understood, but they proceed more rapidly at high than at low temperatures; hence organisms that utilize calcium compounds in their supporting or protective skeletal structures are notably abundant in warm tropical waters, for in this environment shells can be grown faster and heavier than in the cold waters of higher latitudes or the deeper water layers where calcium precipitation is accomplished under great difficulty (Murray, 1895). Among the littoral life we need mention only (1) the marvelous coral faunas which have developed extensive reefs of great geologic importance and which have a wide north-south range in the western sections of the oceans but a narrower range in the eastern sections where the range of warm water is also narrowed, and (2) the beautiful and varied molluscan shells, including the giant clam Tridacna gigas, which may grow to a length of 1.5 m and a weight of 250 kg (551 lb). Conspicuous among the warm-water pelagic animals are the shelled foraminifera and pteropods.

Calcium-precipitating organisms are present in all seas, but their numbers are much reduced in the fauna of the cold polar seas and the shells of those present are relatively more weakly constructed. Some cold-water pteropods construct no shell, living naked, as some species of the beautiful and large Clione. Limacina helicina of Arctic waters does possess a shell but the animal is reduced in size and its shell is very thin. Among the foraminifera, a group apparently very sensitive to temperature conditions, the calcareous-shelled species are replaced in cold northern waters by the arenaceous types, which build shells of sand, fragments of shells, spicules, and so forth, cemented together with noncalcareous cement. Arenaceous types are also characteristic of deep-water foraminifera. In very deep water, therefore water of low temperatures, the skeletons of benthic animals are notably thin and fragile, as exemplified

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by the delicately-shelled Echinoidea of deep water in contrast with their strong-shelled littoral relatives. Deep-water holothuroideans have few or no calcareous plates imbedded in their skin. The carapaces of crustaceans also have little lime. The external skeleton of the giant deep-sea crab Caempfferia caempfferia, for instance, is so weak that the animal would collapse under impact of waves or without the support of water. Barnacles (Scalpellum) of deep water have but incompletely calcified shells. Even internal structures such as the bones of deep-sea fishes are especially fragile and poorly calcified. Calcareous sponges are found from shore to depths of only about 300 to 400 m, and at greater depths are replaced by the siliceous sponges, for example the Venus' flowerbasket Euplectella and the glass rope sponge Hyalonema.

This restricted production of calcareous structures in deep-sea animals can hardly result from a lack of lime for many poorly calcified forms are found where the bottom deposits consist of globigerina ooze which has resulted from precipitation of pelagic foraminifera living in the upper layers. Low temperature is apparently a major cause of the limited production of calcareous structures although the great hydrostatic pressure in deep water may be of importance because it is believed to increase the solubility of calcium carbonate (Buch and Gripenberg, 1932). The absence of violent water movement or even moderately fast flow in the deep sea may also be responsible for the small deposition of calcium by sessile organisms, and the absence of strong motion makes it possible, on the other hand, for many of the fragile-shelled and weak organisms to survive where otherwise they could not exist.

The effect of temperature on biological deposition of calcium carbonate provides a key to the interpretation of temperature conditions and water depths that must have prevailed at periods when certain geological strata of marine origin were laid down in the distant past. The present slight deposition of lime in cold polar regions, as contrasted with what must have occurred when ancient coral reefs were constructed there in Paleozoic times, leads to the theory that these ancient seas must have had a temperature of about 15° to 18°C (Murray, 1895).

Coral-reef formation is a most striking example of marine biological activity, which has attracted wide attention of both laymen and scientists. The coral reefs do not result from spectacular outbursts of activity such as occur among pelagic forms, but rather from the persistent accumulation of calcareous deposits which remain long after the cessation of the biological activity which produced them.

These great structures are outstanding features of the tropical seas. However, since the process of reef formation is a result of biological precipitation of calcium from sea water by corals, the rate of deposition is thermally controlled, as with other organisms. The inequalities of temperature distribution along the continental margins of the tropical

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belt lead to greater reef production in the western portion of the tropical oceans, where the warmer waters accelerate activities of the organisms and therefore favor massive reef formation. In the eastern portion of the ocean, along the west coasts of Central and South America and along the African west coast where cold water upwells, we find that the extent of reef formation is accordingly diminished.

The organisms entering into reef formation are of several types, including chiefly the stony or madreporarian corals, but associated with these are also a number of other calcium-depositing coelenterates such as the Millepora. Very important are the foraminifera and a number of calcareous coralline algae known as the nullipores, of which the red Lithothamneon and the green alga Halimeda are examples. The nullipores in particular contribute vastly to reef formation. In some reefs corals play only a subordinate role.

The reef-producing corals can flourish only in water above about 20°C and are therefore confined to the shallow water of tropical seas. Although conditions are unfavorable for growth below a depth of 50 to 60 m, the slopes of reefs are known to extend to great depths. Also, through examination of material brought up from deep borings (340 m, 1114 ft) within the reefs it is shown that the structure of coral reefs extends to depths far greater than are tolerated by the living animals or plants that enter into the formation of the reefs. Obviously, if the coral fragments occurring at the base of the reefs were laid down in situ, the water level must have been at one time near the level of the base. This implies that the sea bottom on which the reef rests was once at a higher level, or that the sea surface was lower than we now know it.

The subject of reef formation from geological and biological viewpoints has been dealt with in an extensive literature to which the interested reader is referred (see especially Davis, 1928, and Gardiner, 1931). For our purpose it will suffice to state here that the theories which have been advanced largely involve changes in sea level with respect to the substratum on which the coral-building organisms initiated their growth. Some theories assume a sinking of the earth's crust, others a rise in sea level, or a combination of both. Without entering into details on these theories, we shall point out that here is illustrated a problem of the sea the interpretation of which is directly dependent upon an understanding of the organisms involved, for any theory advanced must take into account the biological requirements of the reef-building organisms, which comprise warm, relatively shallow, clear, saline water.

Temperature and Size. There is much evidence, from direct observation of populations obtained from various waters, to indicate that frequently cold-water animals grow to a larger size than do similar animals in warm water. A few examples will suffice to illustrate this point.

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The warm-water epiplankton populations of copepods, the most characteristic of plankton animals, stand in striking contrast to the cold-water populations because of the apparently greater success of the larger species in the cold waters. A fair number of small species of such genera as Oithona, Oncea, Pseudocalanus, and others, of size ranging from about 0.5 to 1.5 mm, do live in cold northern waters and, conversely, a number of large forms, for instance, Eucalanus elongatus (8.0 mm) and Rhincalanus cornutus (3.4 mm) are found in warm waters; however, the warm-water populations are especially characterized by a large number of small species whereas the populations of arctic and boreal waters are mainly composed of great numbers of individuals of a few species, for example, Calanus hyperboreus (10 mm), C. finmarchicus (5.4 mm), C. cristatus (9.3 mm), Eucalanus bungii (8.0 mm). The deep cold waters of lower latitudes are also populated by large forms comparable in size to northern species. The numbers of individuals are, however, relatively fewer.

This tendency to larger size in colder waters is noticeable in related species and even in individuals of the same species. Jespersen (1939) reports that Calanus finmarchicus in Greenland waters forms two size groups, the larger being found particularly in waters of low temperature and the smaller-sized population in warmer surface layers of pronouncedly Atlantic waters. Steuer (1933) found a three-modal curve for body size of three varieties of Pleuromamma taken in the Benguela stream. A dwarf variety (P. minima) occurred in the uppermost, warmest water, a medium-sized race (P. piseki) in the middle layer, and a giant race (P. maxima) in the lower and coldest layer at about 600 m. Steuer has shown also that individuals of the copepods Acartia negligens and A. danae become smaller in transition from the Canary Current to the warm Guinea Stream. Similarly A. danae is larger in the South Equatorial Current, which is mixed with cold water of the Benguela Current.

Some radiolaria, especially the Challengeridae, have been shown to increase in size progressively with depth. In the genus Challengeria eight species can be grouped into three size categories: 0.11 to 0.16 mm, three species; 0.215 to 0.28 mm, three species; and 0.35 to 0.58 mm, two species. These categories correspond to depths of 50 to 400 m, 400 to 1500 m, and 1500 to 5000 m, respectively. Thermal influence on the size of pelagic protozoans is well illustrated also by the ciliates Tintinnoinea collected by the Agassiz Expedition. An analysis of the dimensions of loricae of 1000 individuals of a single species (Tintinnus tenue) of these animals showed that those taken in the Peruvian Current stations with surface temperatures of 19° to 23°C, were predominantly larger than those taken elsewhere at stations with temperatures of 24° to 28°C (Kofoid, 1930).

The effect of this factor on size is indicated also in the plankton fishes. Investigations of the Michael Sars showed that the small deep-sea fishes

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Cyclothone microdon and C. signata increase in size with depth, the former averaging 30 mm at 500 m and 60 mm at 1500 m. The larger size is in part doubtless associated with age, but it is also in keeping with temperature distribution.

Two explanations have been given to account for the increased size of cold-water planktonic forms.

(1) The increased density and viscosity of cold waters enables large forms to keep afloat more successfully in cold than in warm water (p. 822). The matter of overcoming the constant action of gravity is of paramount importance to weakly swimming animals like the smaller crustaceans, as well as to the passively floating radiolaria and many other forms. A size commensurate with viscosity and swimming power is one of the means of overcoming this ever-present tendency to sink. Just how important viscosity may be for delicately adjusted forms is suggested by the fact that the value of the viscosity at 50 m in the Norwegian Sea corresponds to that at 800 m farther south in the Atlantic (Murray and Hjort, 1912).

(2) Lowered temperatures lengthen the time required for poikilothermic animals to reach sexual maturity. Hence, in cold-water forms the delay permits a longer growing period with resultant larger size at maturity. It has been shown that the oxygen consumption of certain nonlocomotory warm-water benthic species is higher than that of related cold-water species with which they were experimentally compared, and this difference in metabolism may have a bearing on the question (Fox, 1936).

The more rapid attainment of sexual maturity in warm-water animals has certain important implications in that it permits a more rapid succession of generations in waters of tropical and subtropical regions. To illustrate this we may refer again to the oyster, Ostrea virginica. In a study of the sexual phases of large numbers of these bivalve molluscs, Coe (1938) found that

From Cape Cod to the Chesapeake Bay, most of the young oysters may be expected to spawn at the age of one year. North of Cape Cod the first spawning is stated to occur more often at the end of the second year, as is the case with some individuals in certain years south of Cape Cod. On the coast of North Carolina and in the Gulf of Mexico, well-nourished individuals of the early set spawn toward the end of their first summer, when only three to four months of age, while those of the later set do not become mature until the following spring.

An increased rate of reproduction is also common in other animals. The more rapid turnover of generations and the more nearly optimum living conditions of lower latitudes, with relative absence of drastic seasonal changes associated with temperature conditions, apparently lead to production of a greater number of species of most animal groups and to

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a greater likelihood of survival of these when once formed than occurs in the more rigorous and selective conditions manifest in the higher latitudes.