Non-genetic adaptation to temperature and salinity

Kurzfassung

Das Phänomen der Adaptation wird aus der Perspektive der Ökologie interpretiert und der Begriff „Adaptation“ definiert als Neueinstellung lebender Systeme im Anschluß an Veränderungen in den Intensitätsmustern von Umweltfaktoren, welche letztlich zu einer relativen Erhöhung der Überlebens-, Vermehrungs- oder Konkurrenzkapazität führt und somit objektiv meßbare „potentielle Vorteile“ im existenzökologischen Sinne beinhaltet. Nichtgenetische Adaptationen (Synonyma: Akklimatisation, Akklimatisierung) vermögen erhebliche Veränderungen in der quantitativen Biologie des Stoffwechsels herbeizuführen. Im zeitlichen Ablauf des Akklimatisationsgeschehens werden drei Phasen unterschieden: Simultanreaktion, Stabilisierung und neuer stationärer Zustand. Eine Simultanreaktion auf plötzliche Umweltveränderungen spielt sich ab in Sekunden, Minuten oder Stunden. Der Vorgang der Stabilisierung dauert (bei marinen Wirbellosen und Fischen) gewöhnlich Tage oder Wochen, wobei oftmals mehr als die Hälfte des „Endanpassungsvolumens“ im allerersten Abschnitt der Stabilisierungsphase bewältigt wird. Die mit dem neuen stationären Zustand verbundenen quantitativen Unterschiede gegenüber der Ausgangssituation werden insbesondere am Beispiel der oberen und unteren Letalgrenzen und der Stoffwechselintensität erläutert. Nichtgenetische Adaptationen können sich aber auch auf andere Funktionen erstrecken, wie etwa Bewegungsaktivität, Vermehrung oder Verhalten und auf strukturelle Bereiche (Körperdimensionen, Organ- und Zellarchitektur, Zellzahl pro Organ etc.). Eine eingehende Beurteilung der quantitativen Aspekte nichtgenetischer Adaptationen erfordert eine Differenzierung zwischen Gesamtvolumen (amount; percentage perfection), Stabilität und Rate. Das Gesamtvolumen erreicht häufig Maximalwerte während der frühen Ontogenie und nimmt danach mit zunehmendem Alter ab. Ähnliches gilt für die Stabilität: Während der frühen Ontogenie erworbene Akklimatisationen erweisen sich häufig als besonders stabil und können im Verlauf des späteren Individualdaseins sogar partiell irreversibel sein. Die Akklimatisationsrate steigt gewöhnlich mit zunehmender Stoffwechselintensität. Vermutlich vollzieht sich eine nichtgenetische Adaptation gegenüber einem Faktor, etwa Salzgehalt, mit unterschiedlicher Geschwindigkeit und unterschiedlichem Nutzeffekt bei verschiedenen Intensitätsmustern eines gleichzeitig einwirkenden zweiten oder dritten Faktors (Temperatur, Sauerstoffgehalt).

Discussion and summary

1. Our present information on non-genetic adaptation of intact aquatic organisms to temperature and salinity does not yet provide a sufficient platform for a detailed analysis. Only a few of the publications available deal with non-genetic adaptation exclusively; many are primarily devoted to other topics. The mechanisms of most types of adjustments appear to be rather complex and are not yet well understood. The net result of non-genetic adaptation is compensation for adversive aspects in a changing environment.

2. Non-genetic adaptation may involve quantitative changes in lethal limits, activity, metabolism, reproduction and other functions as well as in body dimensions, architecture of organs and cells, cell number per organ and in the quantity and activity of enzymes. It practically involves all levels of organismic function and structure. Non-genetic adaptation is not the result of a single process but represents a syndrome. The capacity for non-genetic adaptation depends on the genetic background of the organism involved; it may be different in different ontogenetic stages, such as egg, larva and adult, and may bear relations to metamorphosis and reproduction. There appears to be some evidence that non-genetic adaptations which have been acquired during the most sensitive phase of an individual's life cycle may be transferred to the next generation as non-genetic transmission (e. g.Prosser 1958).

3. There is urgent need for carefully conducted long-term experiments. Much of our present knowledge on non-genetic adaptation has been obtained from organisms kept under inadequate conditions; numerous experiments seem to have been conducted on sick or dying specimens. Even the small amount of information available at this time has therefore to be evaluated with some critical skepticism. Poor conditions and poor health are dangerous prerequisities for the analysis of such a complex and subtle process as is non-genetic adaptation.

4. Assessment of quantitative aspects of non-genetic adaptation requires distinction between its amount, stability and velocity. To illustrate this point, let us consider a euryplastic organism with a considerable capacity for non-genetic adaptation. In such an organism the amount of non-genetic adaptation tends to reach the highest values during early ontogeny and thereafter to decrease gradually with increasing age of the individual. The maximum amount of a given acclimation may only be attainable in individuals born and raised in the test environment. The amount may be expressed in “percentage perfection”. The perfection of a nongenetic adaptation is 100 per cent in the rare case of an “ideal” or “perfect” acclimation, i. e. if the steady-state performance following a significant change in temperature or salinity goes back to its original level after stabilization. In most cases the percentage perfection is much smaller. Thus in the crabPachigrapsus crassipes perfection of acclimation to a seasonal range of about 10°C (Southern California) was calculated byRoberts (1957) from rate-temperature curves for individuals acclimated to experimental temperatures to be about 30 per cent. The degree of stability of a non-genetic adaptation, too, seems to decrease with increasing age: adjustments during early ontogenetic development tend to be more stable than those performed during later periods of ontogeny and may even be — at least in part — irreversible throughout the rest of the life of the individual concerned. Examples areCrangon crangon (Broekema 1941),Gammarus duebeni (Kinne 1953, 1958b),Lebistes reticulatus (Gibson 1954,Fry 1957,Tsukuda &Katayama 1957,Tsukuda 1960),Cyprinodon macularius (Kinne 1962). Reversible acclimations need reinforcement if they are to be maintained. The velocity of non-genetic adaptation tends to increase with increasing rates of metabolism. In the fishCyprinodon macularius, for example, speed of acclimation increases with temperature and seems to be proportional to growth rate: fast-growing fish adapt faster than slow-growing ones (Kinne 1960, 1962).

5. Most authors have considered non-genetic adaptations to a single environmental factor, namely either to temperature or salinity. Organisms, however, react to their total environment rather than to single entities. It is therefore of particular importance to study the combined effects of two or more components of the environment. Very little is presently known about the combined effects of temperature and salinity on the process of non-genetic adaptation (e. g.Dehnel 1960,Todd &Dehnel 1960,Matutani 1962,Alderdice 1963,Kinne 1963b, 1964a, b).McLeese (1956) analyzed the combined effects of temperature, salinity and oxygen on the survival rates of American lobsters (Fig. 8) (see alsoAlderdice 1963), and at the present Symposium,Roberts (1964) reported that the perfection of thermal acclimation of respiration in sunfishLepomis gibbosus becomes a function of day length above temperature of about 10°C.

6. There appears to be some evidence that acclimation to one factor, say salinity, proceeds at different rates and at different efficiencies under different levels of other simultaneous acclimations, for example, to temperature or oxygen (Kinne 1964a, b). Furthermore, inharmonious interrelations between one functional or structural adaptate relative to another may be a fundamental way of limiting the total resulting amount of non-genetic adaptation. The maximum amount of acclimation to a given temperature is presumably only attainable at normal or near optimum salinities, and, conversely, maximum acclimation to salinity is presumably only possible under corresponding temperature conditions.

7. Very little is known about the process of de-adaptation. Does the process of de-acclimation display a similar or a different time course than the respective acclimation? Can de-acclimation from one factor, such as temperature, be initiated or hastened by applying a new stress, such as extreme salinity? De-acclimation may involve active changes and not just a cessation of a given non-genetic adaptation. Thus upon return from high altitude to sea level, erythropoiesis not only stops, but erythrocyte destruction is accelerated (Merino 1950). Apparently, acclimation and de-acclimation are two opposed processes in competition, reaching equilibrium only under constant environmental conditions.

8. The information presented in this paper pertains to reactions of intact, whole individuals. Can we expect cells, tissues or organs removed from multi-cellular animals to preserve and display the full amount of a given non-genetic adaptation acquired in the intact organism? Presumably not, if a substantial part of that acclimation is based on adjustments in organismic integration. But even in other cases, removed cells or organs may often tend to lose part or all of the acclimation acquired due to damages caused by operation procedures. Another important question is whether or not there exists a relationship between the amount of acclimation retained in isolated cells and (a) the level of organismic organization of the test organism (e. g. in the series plant, protozoan, crustacean, fish), or (b) the degree of disturbance caused by the removal of these cells.

9. The amount of cellular acclimation to a given environmental situation may very well be different in different tissues or organs. Thus non-genetic adaptation to changes in salinity may express itself in cells of epidermis, gill or gut rather than in muscle or nerve cells. InCordylophora caspia, for example, acclimation to different salinities results in considerable adjustments in the cells of tentacles, hydranth body and “neck”, while those of the hydrocaulus and stolons remain practically unaffected (Kinne 1958a), and in male rats, cold acclimation causes a remarkable increase in the amount of brown fat, while other tissues do not seem to show such intensive modifications (Smith 1964).