Table Of ContentCONTRIBUTORS
GERARD P. BAERENDS W. S. HOAR
ARTHUR L. DeVRIES P. W. HOCHACHKA
F. E. J. FRY D. J. RANDALL
HENRY GLEITMAN PAUL ROZIN
ARTHUR D. HASLER HORST 0. SCHWASSMA"
G. N. SOMERO
FISH PHYSIOLOGY
Edited by
W. S. HOAR
DEPARTMENT OF ZOOLOGY
UNIVERSITY OF BRITISH COLUMBU
VANCOUVER, CANADA
mnd
D. J. RANDALL
DEPARTMENT OF ZOOLOGY
UNIVERSITY OF BRITISH COLUMBIA
VANCOUVER, CANADA
Volume VI
Environmental Relations
and Behavior
(29
Academic Press New York and London 1971
COPYRIGHT 8 1971, BY AcADEMrc PRESS, INC.
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LIST OF CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors’ contributions begin.
GERARPD. BAERENDS(2 79), Zoological Institute, University of Groningen,
Haren, Holland
ARTHULR. DEVRIES( 157), University of California, San Diego, Scripps
Institute of Oceanography, La Jollu, California
F. E. J. FRY ( l),D epartment of Zoology, University of Toronto, Toronto,
Canada
HENRY GLEITMAN( 191), Department of Psychology, University of
Pennsylvania, Philadelphia, Pennsylvania
ARTHURD . HASLER (429), Department of Zoology, University of
Wisconsin, Madison, Wisconsin
W. S. HOAR (Sll), Department of Zoology, University of British
Columbia, Vancouver, Canada
P. W. HOCHACHKA( N),D epartment of Zoology, University of British
Columbia, Vancouver, Canada
D. J. RANDALL( 511), Department of Zoology, University of British
Columbia, Vancouver, Canada
PAUL ROZIN ( 191) , Department of Psychology, University of Pennsylva-
nia, Philadelphia, Pennsylvania
HORST0 . SCHWASSMAN(N3 71)) Department of Psychology, Dalhousie
University, Halifax, Nova Scotia, Canada
G. N. SOMERO( 99)) Department of Zoology, University of British
Columbia, Vancouver, Canada
ix
PREFACE
Volume VI of this treatise is concerned with the physiological and
behavioral responses of fish to a variety of environmental situations.
The approach is not a detailed analysis of parts of the animal, as in
previous volumes, but treats the fish as an integrated unit interacting
with its environment. Chapters with a similar approach have appeared
in previous volumes (e.g., M. S. Gordon, Hydrostatic Pressure, Volume
IV, pp. 445-464); many contributors to Volumes I-V have discussed the
significance of their observations in terms of the whole animal or even
animal populations. In general, however, previous volumes have been
directed toward an understanding of the physiology of systems within
the animal. Volumes I-V and Volume VI are therefore complementary;
the first five volumes are primarily concerned with an analysis of the
parts while Volume VI is an overview of the whole animal in a chang-
ing and complex environment.
No special consideration of the responses of fish to polluted environ-
ments is included. A detailed analysis of this subject was considered
beyond the terms of reference of this treatise.
The first three chapters of this volume examine physiological and
biochemical adaptations of fish to a variety of environments. In some
respects these chapters also reflect somewhat different approaches
toward an understanding of how animals adapt to their environments.
The next three chapters discuss the extensive literature on behavioral
studies of fishes. Chapter 7 reviews the fascinating problem of fish
migration and orientation. The final chapter is an appendix to all six
volumes and presents what we consider useful information to those
interested in experimenting with fishes.
In conclusion we reiterate our hope that the six volumes of this
treatise on “Fish Physiology” will prove a ready and useful source of
information for those interested in this diverse group of animals.
W. S. HQAR
D. J. RANDALL
xi
1
THE EFFECT OF ENVIRONMENTAL FACTORS
ON THE PHYSIOLOGY OF FISH
F . E . J . FRY
I . Introduction . . . . . . . . . . . 1
A. Metabolism and Activity . . . . . . . . 2
B . Measurement of the Metabolic Rate . . . . . . 3
C . The Relation of Metabolism to Size and Physical Activity . 7
D . Apparatus for the Determination of Metabolic Rate . . . 10
E . Acclimation . . . . . . . . . . . 14
F. A Classification of the Environment . . . . . . 15
I1 . Lethal Factors . . . . . . . . . . . 18
A. Determination of Lethal Effects . . . . . . . 21
B . Toxicity Studies . . . . . . . . . . 36
111 . Controlling Factors . . . . . . . . . . 38
A . Formulas Relating Temperature to Metabolism and Activity . 40
. .
B Active and Standard Metabolism in Relation to Temperature 42
C . Acclimation to Controlling Factors . . . . . . 47
IV. Limiting Factors . . . . . . . . . . . 50
A . Acclimation to Low Oxygen . . . . . . . 53
B . Oxygen Concentration and Metabolic Rate . . . . 56
C . Combinations of Oxygen and Carbon Dioxide . . . . 59
D . Interaction of Limiting and Controlling Factors . . . 65
V . Masking Factors . . . . . . . . . . . 67
A. Cost of Ion-Osmoregulation . . . . . . . . 67
B. Thermoregulation in Fish . . . . . . . . 73
VI . Directive Factors . . . . . . . . . . 75
A. Reactions to Dissolved Substances . . . . . . 77
B . Temperature Selection . . . . . . . . . 79
VII . Recapitulation . . . . . . . . . . . 84
References . . . . . . . . . . . . . 87
.
I INTRODUCTION
The study of animal function is organized more or less under three
heads which in everyday language are. as applied to a machine. what it
1
2 F. E. J. FRY
can do, how it works, and what makes it go. Insofar as fields of study
can be classified in biology these divisions of the subject are ordinarily
considered to be autecology, physiology, and biochemistry, with a great
deal of individual taste governing the label any particular worker may
choose for himself. The subject of this chapter is what fish can do in
relation to their environment and therefore largely autecology.
The organism can be taken to be an open system (von Bertalanffy,
1950), suitably walled off from its milieu, through which energy flows
by appropriate entrances and exits. The organism uses this energy to
maintain and extend its being. The energy comes from the environment,
and further the environment sets to a large degree the conditions under
which the organism uses the energy it has assimilated, but all organisms
have regulatory powers and bargain with the environment in regard to
the extent they make use of the energy they have gained. Such bargain-
ing involves the use of some energy for regulation against the environ-
ment to free the rest for the organism’s other activities.
Thus the prime subject of this chapter will be the action of the en-
vironment on metabolism and the effects of this action on the activity
of the organism.
A. Metabolism and Activity
A careful distinction will be made here in the usage of the terms
metabolism and activity. Metabolism as used here is catabolism as
ordinarily understood, that is, the sum of the reactions which yield the
energy the organism utilizes. Activities are what the organism does with
the energy derived from metabolism. Thus activities are such processes
as running or fighting or other manifestations of the energy released by
metabolism. These manifestations are not all movements; growth is
activity and so is excretion. By this definition anabolism is an activity.
While the influence of the environment is on metabolism, the effect of
that influence is displayed through the activity of the organism whose
metabolism has been so affected.
The purpose of belaboring the distinction between metabolism and
activity here is not to introduce a novel thought, for these generalities
are what we all recognize, but rather to provide a consistent treatment
of the whole organism in relation to its biochemical basis. Activity is
fundamentally the result of transformation of energy from one form to
another and the appkation of that energy to a given performance. Two
generalizations arise from these circumstances. First, all the energy
released will not likely be applied to the final outcome which is the
1. EFFECT OF ENVIRONMENTAL FACTORS 3
object of its release. The organism will take its levy for its maintenance
as a system, and there will be the ancillary costs of supply and disposal
of the metabolites which pass through the system. Second, performance
is qualitatively different from the power which produces it and there
need not be any simple proportionality between the measures taken of
the two.
These circumstances will be recognized here by considering the
difference between resting and active metabolic rates, which will be
termcd “scope for activity,” as being the power available for activity, and,
where appropriate, relations will be sought between activity and scope.
These concepts are, of course, regularly applied to honioiotherms by
those interested in animal production (e.g., Brody, 1945) where the
costs and conscquences of thermoregulation are so prominent and have
been simply transferred to poikilotherms over the past quarter century.
B. Measurement of the Metabolic Rate
The metabolic rate of fish has almost universally been measured by
determining oxygen consumption. The fundamental method of measuring
heat production has been applied (e.g., Davies, 1966) but probably
never will be suitable for measurements required for environmental
physiology.
It cannot be assumed that all fish are obligate aerobes and that a
measure of oxygen consumption is always a measure of the metabolic
rate. Coulter (1967) reported that extensive catches of fish are regularly
taken in oxygen-poor water in Lake Tanganyika under circumstances
which suggest they are resident there. The goldfish (Kutty, 196th) can
live for months with a respiratory quotient of 2, and there are the
dramatic reports of Blaika (1958) and Mathur (1967) on extensive
survival of fish under completely anaerobic conditions.
The newer methods of easy determination of carbon dioxide in water
should soon be rapidly applied to the determination of the respiratory
quotient (e.g., R. W. Morris, 1967) although, as yet, the margin of error
in them requires to be narrowed. At present the error inherent in the
new methods is of the order of twice that for determinations with the
Van Slyke apparatus or by distillation (e.g., Maros et al., 1961).
Three levels of metabolism will be distinguished here. Following the
usage now current among a number of fisheries workers, these will be
termed “standard,” “routine,” and “active” levels of metabolism. Standard
metabolism is an approximation of the minimum rate for the intact
organism. It is preferably determined as the value found at zero activity
4 F. E. J. FRY
by relating metabolic rate to random physical activity in fish in the post-
absorptive state ( e.g., Beamish and Mookherjii, 1964; Spoor, 1946). The
fish should be able to swim freely in the respiration chamber while
protected from outside disturbance and should have been in the chamber
long enough to recover from the effects of transfer to it. It may also be
important that the chamber is supplied with water from the aquarium
in which the fish was living. Foreign water may provide disturbing chem-
ical stimuli or perhaps more importantly may lack the familiar chemical
milieu of the home tank, Standard metabolism can also be determined by
extrapolation to zero activity from determinations at various levels of
forced activity (e.g., Brett, 1964). The routine rate of metabolism is the
mean rate observed in fish whose metabolic rate is influenced by random
activity under experimental conditions in which movements are presum-
ably somewhat restricted and the fish protected from outside stimuli. The
value has usually been given only for the normal working hours of the
experimenter (e.g., Beamish, 1964a). Active metabolism is the maximum
sustained rate for a fish swimming steadily.
Standard and active metabolism are determined to permit calculation
of scope for activity. Routine metabolism is largely to be considered as a
measure of the degree of random activity and is discussed in Section VI.
Various types of apparatus used in such determinations are discussed
below, together with comments on experimental precautions. Most
measures of metabolism have been measurements of routine metabolism.
Standard and active metabolism have not yet often been measured, and
the limits of these have been still less often well worked out.
Figure 1 shows determinations of the metabolic rate of the goldfish,
Carassius auratus, at 20°C by various workers in the same laboratory at
various times over a number of years. Figure 1A shows oxygen consump-
tion and Fig. 1B CO, output. For the sake of clarity, Kutty’s points for
oxygen consumption are not shown but the number of his readings under
forced activity can be inferred from the number of points in Fig. 1B since
he made determinations of the respiratory quotient. His curve for routine
metabolism is based on 35 points. Smit’s data (1965) are illustrative
material based on a single fish. There are three salient points to be con-
sidered in Fig. 1A:
(1) The dots which represent oxygen consumption during routine
activity show how high the metaboIic rate can go when a fish is randomIy
active within the confines of a respiration chamber. The routine respira-
tion rate as shown by the mean of these values approaches half the active
respiration rate.
(2) An extrapolation from either forced or random activity to zero
1. EFFECT OF ENVIRONMENTAL FACTORS 5
I
’@‘k
Theoreticol oerobic
\
Kutty forced tirstLho~limUrn
02
a2
Kutty forced long 0”
term k t r s ton dord - 0
50
, ” Smit ditto
Fry’s respiromdter
’
Bla’zka’s respirometer
6’- Smit standard
~o Beamish and Mookherlii standard
I 1 I
0 20 40 0 40 80 100
Swimming speed (cm/sec)
Fig. 1. Various measures of metabolism of the goldfish, Carassiur aurutus,
under conditions of random and forced activity at 20OC. (A) Oxygen consumption;
(B) carbon dioxide production. Data of Basu (1959), Beamish and Mookherjii
(1964), C. N. Cook (personal communication in Fry, 1987), Kutty (1968a), and
Smit (1965). Kutty’s data for oxygen consumption under forced activity are omitted
from A but are based on the same number of observations as are shown by the
points in B. For further explanation see text.
activity gives a similar value for standard metabolism if the fish are not
disturbed.
(3) A major problem in the measurement of metabolism of fish is the
wide range of values that may be obtained for a given fish in the same
state of overt physical activity. A fish resting quietly may be consuming
oxygen at a given rate from its standard to well over half its maximum
level. Ordinarily a fish need only be moved from its bath to the respira-
tion chamber to elicit almost its active metabolic rate. Cook’s data illus-
trate this phenomenon in Fig. 1. Her data are for the first 15 min after the
fish were transferred from their acclimation tank to the respiration cham-
ber. The effect of swimming is to somewhat increase oxygen uptake in
an excited fish, possibly by facilitating venous return, but more than half
the extrapolated maximum rate of oxygen consumption associated with
the most vigorous sustained activity can be displayed by the goldfish with
