ABSTRACT
Many exaggerated statements have been made, and too often uncritically repeated, concerning the temperatures at which animals and plants have been found in hot springs. To throw light on this subject, the author undertook two expeditions—in the summer of 1937 and the winter of 1938–9—to study the hot springs at Hammam Meskoutine, Algeria.
These springs and some of the animals in them were originally described by Gervais (1849) and later by Blanchard (1903), but neither author gave them more than a casual examination. Since they are not sulphurous or saline they constitute a habitat in which the only special feature is the high temperature; furthermore, since they present a graded series of temperatures from 95° C. downwards, their fauna is living in a permanent temperature gradient. These two features make them particularly suitable for the study of the upper temperature limits for life.
An attempt was also made to discover whether the hot spring animals differ physiologically from normal forms and if so wherein this difference lies. This is a subject about which there is very scanty information in the literature, except in the case of marine animals for which physiological races, adapted to different environmental temperatures, have been discovered by Mayer (1914), Huntsman & Sparks (1924), Fox (1936, 1938), and Fox & Wingfield (1937).
PART-I. MAXIMUM TEMPERATURES AT WHICH ANIMALS AND PLANTS WERE FOUND
The hot springs of Hammam Meskoutine rise at various temperatures between 50 and 90° C. in the beds of travertine (95 % CaCO3) which they have deposited. The most spectacular series of springs rises on a plateau, and the water flows over a gleaming white precipice as a steaming cascade. The water contains 1·4 parts per thousand of salts. A typical analysis of the water and its deposit is given in Table I. At its source the pH of the water is about 7·0, but it rises to 8·5, as the water in coolihg gives off CO2 and deposits CaCO3. The hot water flows into a small stream, the Oued Chedakra, which it heats to 60–65° C. As the heated stream flows away it gradually cools, producing a series of habitats similar except that their temperatures vary from 65 to 20° C. This series is repeated several times in the Oued Chedakra and also in a number of irrigation canals drawn from it, so that the range of any animal could be confirmed in a series of gradients. Finally, the stream flows into a small river, the Oued Bou Hamdam, which in summer is heated to 40°C., but in winter, when in flood, is unaffected.
The sketch map (Fig. 1) shows the position of the chief springs, the course of the Oued Chedakra and the summer temperatures at various points along it. Further details of topography and geology will be found in books by Piot (1893) and Fiorini (1935).
(1) Plants
No life was found above 58° C. (bacteria were not looked for), but at this temperature a carpet of blue-green algae was noticeable. This carpet was continuous down to 40–38° C. where it thinned out. The principal species found, with their limits of distribution, were as follows :
These and other species of Oscillatoria have already been recorded in other North African hot springs (Seurat & Frémy, 1937), but only at a considerably lower temperature (38° C.). Copeland (1936), in an extensive investigation of the bluegreen algae of the Yellowstone Park, also records these species of Oscillaioria and Spirulina at approximately the same temperatures as the present author. The highest temperatures at which Copeland found any life where :
It should be noted that these figures refer to siliceous waters. In calcareous springs, such as the one at Hammam Meskoutine, the maximum temperatures are about 15–20° C. lower (Setchell, 1903).
(2) Animals
Table II shows the principal animals from truly thermal waters and the maximum temperature at which each was consistently found. 38°C. was arbitrarily chosen as the lowest temperature at which the stream could be considered thermal, since some of the small pools into which the Bou Hamdam dries up in summer are heated by the sun to a temperature just below this, viz. 36° C. They still differ, however, from thermal waters of the same temperature in their diurnal and seasonal changes and in the presence of cool depths to which animals can retire from the heated surface.
About this temperature (38–35° C.) the character of the stream changes owing to the disappearance of the algal carpet and the appearance in large numbers of the species forming the general freshwater fauna of the district, viz. ephemerid and dragonfly nymphs, caddis worms, gyrinid beetles, water skaters, corixids, rotifers, fresh-water oligochaetes, gammarids and free-living nematodes. To the human hand, too, 38–35° C. marked the transition from “hot” to “lukewarm”.
Setchell (1903), writing of the Yellowstone Park, counts as truly thermal waters only those with temperatures above 43–45° C., but does not give his reasons. He emphasizes the necessity of taking temperatures exactly where animals and plants are found, since the bottom of a deep pool or the edges of a sluggish stream may be at a lower temperature than the rest. This practice was invariably observed by the present author. In addition, a careful distinction was drawn between the maximum temperature at which specimens were found occasionally or in small numbers, and the optimum temperature at which they live habitually. This distinction applied particularly to the two most interesting animals in the list, Cypris balnearia and Bidessus signatellus, which are species confined to thermal waters. The other animals of special interest are Barbus callensis and Potamon edulis, which are widely distributed in the surrounding cool streams but have resistant races in the hot springs. The distribution and physiology of these animals will be discussed in the second part of this paper.
(3) The upper temperature limits for life
Previous extensive study of hot spring animals has been made by Issel (1901, 1906, 1908, 1910) for the Italian springs, and by Brues (1924, 1928, 1932) for the American springs. The latter gives a very complete survey of the literature. His results indicate that 41° C. is the upper limit for vertebrates and 45°C. for most invertebrates, while a few groups (ostracods and hydracarines) are found up to 50–51° C. These results agree very closely with mine.
From a careful investigation of the literature I have drawn up, the following table of the maximum temperatures at which various animal groups have authentically been found (Table III). It should be noted, however, that these may represent merely temporary maxima and the animals listed may not be able to survive prolonged exposure to these temperatures. This question is discussed in connexion with the death-point of Cypris (see below).
PART II. THE ADAPTATION OF HOT SPRING ANIMALS TO THEIR ENVIRONMENT
Several authors (Issel, 1906; Vouk, 1923; Brues, 1932; Copeland, 1936) have attempted to classify the fauna of hot springs according to their assumed origin, e.g. marine, tropical,. primeval, fresh water. The assumption underlying this method of grouping does not rest on experiment, so this classification throws no light on the more interesting question: How are animals able to withstand the abnormally high temperatures of hot springs? The author has divided the Meskoutine fauna into the following groups according to physiological differences observed during experiments done on the spot with animals straight from the stream :
Those species common in the surrounding fresh water which are merely living nearer their thermal death-point.
Those species common in the surrounding fresh water which have more resistant physiological races living in the hot springs.
Those species confined to hot springs.
(1) Animals living nearer their thermal death-point
Of the animals on which death-point experiments were performed only frogs and tadpoles fell into this group, but most of the other animals whose range ends about 37–39° C. probably belong here too.
The frogs and tadpoles were immersed in water of constant high temperature until they died ; the frogs were allowed to keep their noses out of water so that they would not suffer from oxygen lack. From a series of such experiments the highest temperature was determined at which they could live without showing signs of discomfort for an arbitrary period of 1 hr.
Frogs taken from cool water at 23°C. lived uninjured in the laboratory at 38° C., but heat rigor set in after a few minutes at 39° C. This is in accordance with the observed behaviour in the field of the hot stream frogs. They spend most of their time sitting on the bank, only diving in when disturbed and remaining immersed for a period which varies inversely with the temperature of the water. Table IV shows this correlation.
The death-points of the tadpoles are shown in Fig. 2. The numbers are too few to enable definite conclusions to be drawn except that the larvae are more resistant than the adults. There is no well-marked indication of physiological races differing in their death-points. In any case, frogs and tadpoles, being only temporary inhabitants of water, are not so interesting in this connexion as fish, which live there permanently.
(2) Adaptive Physiological races
Barbels (Barbus callensis) were abundant in a large pool at a uniform summer temperature of 37° C. ; they made occasional excursions into water at 38° C. but rigorously avoided higher temperatures. They were also present in large numbers in all streams at temperatures below 37° C. This distribution is shown in Fig.1. The minimum temperature at which they were found was 8° C., in winter.
It was found that the death temperature of the fish varied according to the temperature at which they lived. For these experiments a gradually rising temperature was used rather than sudden immersion in hot water in order that the conditions might more nearly approach those naturally experienced by the fish. The temperature was raised rapidly to 30° C. and thereafter very slowly (between I and 2° C. per hour), so that at any one temperature the fish had time to regain its balance lost, presumably, by the expansion of the gas in its swim bladder.
Fish were taken from three different habitats :
A portion of the Oued Chedakra (see Fig. 1), including a hot pool and the stream flowing out of it along which the temperature range was nearly the same summer and winter (July 30–36° C. ; January 28–34° C.). Experiments in July and January gave similar results.
A part of the Bou Hamdam several miles below the entry of the Chedakra which was unaffected by hot spring water; January temperature 8–10°C. The July temperature was not taken at this exact spot, but by comparison with other parts of the river it was probably 15–20° C. Death-points were taken in January only.
The Bou Hamdam near the entry of the Chedakra (see Fig. 1). Here the July temperature was 26–30° C., in December it was 19–20° C., while in January, when the winter rains had begun and the river was in flood, the temperature was 8–9° C. Death-points were taken both in December and January, but the same range of variation was shown in each batch.
The results obtained are shown in Fig. 3. In each case a wide range of sizes was used, but no distinct correlation between size and death-point was observed.
It is clear that temperature is the factor limiting the upper range of the fish, which, in the hottest places, are living dangerously near to their thermal deathpoint.
It is also clear that the fish from the hot water are more resistant to high temperatures (death-points 37–40° C.) than those from the cold water (death-points 31–33° C.). Since the range of death-points for the “cold” fish—which are the normal form—is so small, the “hot” fish cannot represent merely the result of selection by temperature from a mixed population. But the wide range of variation in the “medium” group may represent a direct acclimatizing effect due to the high, or to the high and variable, temperature, and from this group the most resistant individuals may have been selected to colonize the hottest waters.
Similar but less conclusive results were obtained with crabs (see Fig. 4). Those from a temperature of 32-36° C. had a death-point in both summer and winter of 39·5–40° C.; those taken in summer from 20 to 25° C. died at 38–39° C. The crab is like the frog in not spending all its time in the hot water; it lives in burrows in the bank at a slightly lower temperature than the stream itself, only making occasional excursions into the latter, presumably for feeding. It can always avoid too high a temperature by crawling out of the water; experiment showed that it could live out of water for at least 17 days.
(3) Specialized hot spring animals
Bidessus signatellus
These beetles were found actively moving on the felt of algae between 45 and 33° C. They were only found once below this temperature in a stream which had suddenly cooled to 28° C. Larvae were found only where the adults were most abundant, viz. 41–38° C. Death-points were difficult to determine, since the beetles tended to avoid a lethal temperature by crawling out of the water. Also it was not easy to decide when an animal was dead because death was preceded by a period of reversible heat rigor. Death always occurred at 45° C., however, after times ranging from 20 to 75 min., so that temperature is clearly the upper limiting factor in the field.
The nature of the lower limit is not clear. The limiting factor is not temperature, since the beetles were unaffected even by a temperature as low as 11° C. although below this chill coma was produced. Recovery occurred on reheating to 17·5–23°C. according to the length of coma. Complete recovery still occurred after more than 5 hr. below 7° C.
Cypris balnearia
This species was incompletely described by Moniez (1893). It is being redescribed by Klie under the name of Heterocypris.
The distribution of Cypris at various temperatures in the field, and the times for death for sudden immersion at various temperatures in the laboratory, are shown in Tables V and VI. A comparison of these two tables shows that whereas Cypris dies in the laboratory at 49° C. it is actually found in the field above this temperature, viz. up to 51–5° C. A possible explanation of this anomaly is as follows. It was shown in the laboratory (see Table VI) that temperatures between 49 and 52° C. were lethal only after some hours. Since some hundreds of individuals tested all had the same thermal death-point, it is unlikely that the few found in the field above 48° C. are members of a specially resistant race. It appears much more probable that they are individuals which have made temporary excursions from the cooler regions near the banks, where the majority are packed in dense masses, towards the warmer centre of the stream.
Resistance to heat seems to be correlated with resistance to oxygen lack, since it took 3 days to kill animals in boiled water at 20–30° C. in which no oxygen could be detected by the Winkler method.
The nature of the lower limit again does not appear to be a matter of temperature. Cypris lived in the laboratory for at least 17 days in water at room temperature (20–30° C.), although its activity was much reduced. Chill coma occurred at 17·5° C., and on reheating recovery took place, even after the animals had been kept for 4 hr. at a temperature below 7° C.
Possibly the abrupt disappearance of Cypris at 38·5° C. in the field is connected with the thinning out of the algae on which it feeds, or with the appearance at this temperature of animals which may feed upon it, e.g. fish, frogs and tadpoles, crabs and dragonfly nymphs.
DISCUSSION
The first experimental work with a bearing on the physiology of hot spring animals was done by Plateau (1872) on fresh-water arthropods. Although he confined his actual death-point experiments to normal cool-water forms, he collected specimens of the same species from a number of French hot springs and found that the temperatures of these springs were in no case higher than the death-points of his cool-water forms. Even in the absence of data on the death-points of the hot spring specimens it seems likely that this is not a case of physiological adaptation but merely of normal fresh-water forms living at temperatures nearer their deathpoints.
More recently, Lutz (1931) has made some observations on the animal life of thermal waters in the Yellowstone Park. He convinced himself that temperature, and not oxygen lack or pH, is the upper limiting factor and showed two ways in which the factor operates. Either the animals deliberately avoid a temperature too high for them—as the present author observed Barbus avoiding a temperature above 38° C.—or if they overstep the limit they are inactivated by heat rigor and are washed downstream to a cooler portion where they can recover. This latter phenomenon may occur in the case of the Cypris at Hammam Meskoutine but was not actually observed.
Other authors have shown in marine animals the existence of physiological races with their death-points adjusted to their habitats, comparable with the case of Barbus discussed here. Mayer (1914), in particular, has shown that the jelly fish Aurelia aurita can live between — 1 and 29° C. off Nova Scotia, where the average summer sea temperature is 14°C., while in Florida, where the summer sea temperature is 29°C., the lower and upper limits are raised to 8 and 37° C. respectively. Huntsman & Sparks (1924) have demonstrated some correlation between death temperature and temperature of habitat in the case of the genus Raia. The more northern species R. erinacea, dies at 29·6° C., and the less northern R. radiata at 26·7° C. They found a similar correlation within the species Pseudopleuronectes americanas, of which small specimens from warm shallow water die at 30° C., while large specimens from deeper cool water die at 28° C.
Finally, Hindle (1932) has made an interesting observation on an Amoeba found in a hot spring at Dax near Bordeaux at 54° C. It would live in culture only between 37 and 54° C., remaining encysted from 54 to 60 and below 37° C. This is a hot-spring animal with an even more specialized physiology than the Cypris and Bidessus discussed here. In all three cases the indications are that adaptation to high temperatures precludes activity at low temperatures.
SUMMARY
A description is given of the hot springs of Hammam Meskoutine, Algeria, and the principal animals and plants found living in them above a temperature of 38°C.
Life was found up to the following maximum temperatures: plants (bluegreen algae), 58° C.; animals (Cypris balnearia), 51·5° C.
A comparison between the death-points of the principal animals and the temperatures at which they were living shows :
That some animals (Cypris balnearia and Bidessus signatellus) are confined to thermal waters.
That some animals can exist, for short periods, at temperatures above their eventual thermal death-points (Cypris balnearia and Rana ridibunda).
That some animals have death-points which vary with the temperatures at which they live (Barbus callensis and Potamon edulis).
ACKNOWLEDGEMENTS
The second expedition was financed by a Government Grant from the Royal Society.
The author wishes to express his gratitude to his wife who has assisted him at every stage in the investigation, to Prof. James Gray for his unceasing encouragement, to Mr George Bartmann, for the loan of collecting nets, and to Herr W. Klie and the staff of the Natural History Museum for the identification of material.