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The influence of body weight on gas exchange in the air-breathing fish, Clarias batrachus

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Title:
The influence of body weight on gas exchange in the air-breathing fish, Clarias batrachus
Creator:
Jordan, Jill Ann, 1944-
Publication Date:
Language:
English
Physical Description:
viii, 63 leaves. : illus. ; 28 cm.

Subjects

Subjects / Keywords:
Air ( jstor )
Body weight ( jstor )
Breathing ( jstor )
Fish ( jstor )
Gills ( jstor )
Oxygen ( jstor )
Oxygen partial pressure ( jstor )
Respiration ( jstor )
Surface areas ( jstor )
Water uptake ( jstor )
Body weight ( lcsh )
Catfishes ( lcsh )
Dissertations, Academic -- Zoology -- UF
Fishes -- Physiology ( lcsh )
Respiration ( lcsh )
Zoology thesis Ph. D
Miami metropolitan area ( local )
Genre:
bibliography ( marcgt )
non-fiction ( marcgt )

Notes

Bibliography:
Bibliography: leaves 60-62
General Note:
Typescript.
General Note:
Thesis -- University of Florida.
General Note:
Vita.

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University of Florida
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University of Florida
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Copyright [name of dissertation author]. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
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AA00004929_00001 ( sobekcm )

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Full Text





















THE INFLUENCE OF BODY WEIGHT ON GAS EXCHANGE IN
THE AIR-BREATHING FISH, Clarias batrachus










By





JILL ANN JORDAN


A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF
THE UNIVERSITY OF FLORIDA
IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY







UNIVERSITY OF FLORIDA
1973


_I




THE INFLUENCE OF BODY WEIGHT ON GAS EXCHANGE IN
THE AIR-BREATHING FISH, Ciarias batrachus
By
JILL ANN JORDAN
A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF
THE UNIVERSITY OF FLORIDA
IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
1973


ACKNOWLEDGEMENTS
I gratefully acknowledge the help of the many people who
contributed to this study. Special thanks go to Vernon Ogilvie
of the Florida Game and Fresh Water Fish Commission who assisted
in collecting specimens and provided much useful information on
the biology of Ciaras in Florida, and to Don Goodman who assisted
in collecting, setting up experiments, and proof-reading the manu
script.
I am indebted -to Dr. Brian McNab for his assistance and criticisms
and for enduring the clutter and floor-to-ceiling mud in his laboratory,
and to Drs. Frank Nordlie, John Kaufmann, Pierce Brodkorb, Hugh
Popenoe and Stephen Zam for criticism of the manuscript and use of
space and materials. Dr. Gordon Ultsch provided much valuable in
formation on the techniques used in the study.
Mr. Paul Laessle provided valuable counsel on the preparation of
the figures, and Ms. Donna Gillis typed the manuscript and aided in
the completion of the final details of preparation.


TABLE OF CONTENTS
Page
Ac knc wl edgements ^
List of Tables iv
List of Figures v
Abstract vii
Introduction 1
Materials and Methods 7
Results 10
Discussion 37
Summary 58
Bibliography 60
Biographical Sketch 63
iii


LIST OF TABLES
Page
1. The Metabolic Rate of Various Air-Breathing Fishes
(and Ictalurus nebulosus) Under Varying
Experimental Conditions 39
2. Oxygen Capacities of the Blood of Representative
Air-Breathing Fishes 43
iv


LIST OF FIGURES
Page
1. Metabolic rate of forcibly submerged £. batrachus
as a function of body weight 12
2. Metabolic rate of air exposed £. batrachus as a
function of body weight 14
3. Metabolic rate of £. batrachus, in water with access
to air, as a function of body weight 16
4. Metabolic rates of £. batrachus (forcibly submerged,
air exposed, water with access to air) and poikilotherms
(from Hemmingsen, 1960) as a function of body weight. ... 18
5. Metabolic rate of £. batrachus weighing 42 g as a
function of oxygen tension 21
6. Metabolic rate of £. batrachus weighing 77 and 83 g
as a function of oxygen tension 23
7. Metabolic rate of £. batrachus weighing 172, 195 and 206 g
as a function of oxygen tension 25
8. Relationship between oxygen uptake from air and oxygen
tension of the water in C_. batrachus weighing
30-71 g 28
9. Relationship between oxygen uptake from air and oxygen
tension of the water in £. batrachus weighing
141-210 g 30
10. Diurnal and nocturnal surfacing frequency as a
function of body weight 33
11. Average number of surfacings per hour as a function
of time of day in air-saturated water and nitrogen-
saturated water 35
12. Gill surface area as a function of body weight for
various aquatic respiring teleosts (from Muir, 1969)
and £. batrachus (from Saxena, 1966) 41
v


13. Critical oxygen tension of C_. batrachus and two
salamanders, Siren (from Ultsch, 1972) and
Desmognathus (from Beckenbach, 1969), as a
function of body weight 47
14. Gill surface area of C^. batrachus as a function
of body weight (from Saxena, 1966) 51
15. Buffering capacity of blood of selected vertebrates
at 25C (from Howell, 1970, and Rahn, 1967) 55
vi


Abstract of Dissertation Presented to the Graduate Council
of the University of Florida in Partial Fulfillment of the Requirements
for the Degree of Doctor of Philosophy
THE INFLUENCE OF BODY WEIGHT ON GAS EXCHANGE IN
THE AIR-BREATHING FISH, Clarias batrachus
By
Jill Ann Jordan
June, 1973
Chairman: Dr. B. K. McNab
Major Department: Zoology
Aerial respiration and its capacity for terrestrial locomotion
have enabled Clarias batrachus, a clariid catfish from southern
Asia, to establish a large breeding population in southeastern
Florida. Clarias batrachus is a facultative air breather, and at
aquatic oxygen tensions exceeding 40 mmHg, an oxygen regulator.
The rate of metabolism of Clarias varies as a function of
weight, and access to air. Aerobic metabolism is primarily utilized,
even during forcible submergence when the metabolic rate declines.
Clarias, a terrestrially active fish under certain environmental
conditions, shows no metabolic reduction upon emersion.
The aquatic oxygen tension below which Clarias becomes an
oxygen conformer is directly proportional to body weight, and about
1/3 the value for bimodally breathing salamanders; the disparity is
presumably the result of the greater surface area for gaseous exchange
in Clarias.
The number of air breaths per unit time doubles at night and
is inversely proportional to body weight.
vii


The sensitivity of its naked skin to desiccation and the low
bicarbonate buffering capacity of its blood limit the terrestrial
activity of Ciaras to rainy nights when a cutaneous film of water
can be maintained.
viii


INTRODUCTION
The transition from aquatic to aerial breathing was one of the
most important events in vertebrate evolution. Air breathing has
evolved in numerous taxonomically unrelated groups of teleosts, and
has produced a remarkable degree of convergence in these fishes.
Bimodal breathers run the respiratory gamut from facultative air
breathers that can survive indefinitely on the oxygen dissolved in
water (except in times of severe oxygen stress), to obligate air
breathers (such as Electrophorus, Lepidosiren, and Protopterus)
that will drown when denied access to air; hence this is an excellent
group in which to study the physiological modifications imposed by
bimodal respiration. One such bimodally breathing teleost, Clarias
batrachus, the "walking catfish," is the subject of this study.
Air breathing has enabled this exotic introduction from southern
Asia to become one of the dominant fishes in southeastern Florida;
hence this species is an interesting form in which to study some
of the aspects of bimodal respiration that have contributed to
its success.
The two respiratory media, water and air, differ greatly in
their physical properties, imposing very different morphological
and physiological adaptations on the structure and function of
respiratory surfaces. Water is a medium that often offers marginal
conditions for gas exchange. It is frequently oxygen deficient.
At 25C, oxygen attains only 1/35 the concentration in water that
1


2
it does in air, but carbon dioxide is 27 times more soluble in water
than oxygen, and may reach concentrations greatly in excess of
aerial values. Consequently water breathers must ventilate much
larger volumes of a denser medium than air breathers for a similar
oxygen uptake. Air, In contrast, with its high partial pressure
of oxygen offers a favorable diffusion gradient but requires
significant structural support for respiratory surfaces. Furthermore,
an atmospheric humidity below saturation will cause evaporation from
the epithelial surfaces that must remain moist for gas exchange.
Therefore a premium is placed upon structures protected within the
body for aerial gas exchange. Obligate air breathers also must have
an increased efficiency of the internal buffering system because of
the elevated internal carbon dioxide tensions.
Since the differences in gaseous composition between air
and water increase with temperature, it is not surprising that
the majority of extant air-breathing fishes live in tropical fresh-
waters. These relatively warm waters usually have low oxygen and
high carbon dioxide concentrations, due to the lack of turnover
(because there is little wind disturbance and night temperatures
are not cool enough), the reduction of aquatic photosynthetic
activity because of shading, and the high B.O.D. of such waters.
Only a few temperate fresh-water species exhibit air breathing
(Lepisosteus, Amia, and Umbra). Johansen (1970) demonstrated that
air breathing in Amia calva increases at higher temperatures. The
few marine air-breathing fish [some members of the families
Gobiidae (including the mud skippers) and Blennidae, the clingfish
I


3
Sicyases (Gordon et al., 1970), the eel, Anguilla (Berg and Steen,
1965), and tarpons (Elopidae)] are mostly estuarine secies and
probably often encounter deoxygenated water in areas of organic
decomposition such as mud flats, mangroves and vegetation mats.
i
Air breathing has enabled many of these fish to not only
inhabit water with unfavorable gas tensions, but even to leave the
water and spend part of their time on land. Certain fish, such as
Anguilla (Berg and Steen, 1965), Symbranchus (Johansen, 1966),
Ciarlas batrachus (Smith, 1945; Das, 1927), Saccobranchus "
Heteropneustes, Anabas and Ophiocephalus (Das, 1927), frequently
make night sojourns from pond to pond through moist grass. Some
of these fishes are thought to feed while making these excursions.
The Chilean clingfish, Sicyases sanguinensis (Gordon et al., 1970)
rests on rocks in the inter-tidal splash zone, while the more
active mudskipper, Periophthalmus, actually leaves the water to
escape predators and to feed (Johansen, 1970). Other fish, such
as African species of Ciarlas may move from drying pools to permanent
bodies of water. Desiccation is a problem faced by most of these
fish when they leave the water, hence the extent of these land
excursions is a function of weather conditions, time of day,
and physical conditions of the area.
In India (Das, 1927) and in south Florida (Ogilvie, personal
communication), great numbers of Ciarlas batrachus migrate in the
rainy season, presumably for feeding purposes. Mookerjee and
Mazumdar (1950) reported that Ciarlas batrachus rarely migrates


4
by a land route like Anabas, but frequently migrates in shallow
running water. This account corroborates descriptions of its
behavior in south Florida, and some of the conclusions reached in
this study.
If they are unable to escape a drying pool, certain air-breath
ing fish burrow into the mud and become dormant. Estivation has been
reported for Ciaras (Das, 1927; Sterba, 1963), Saccobranchus
(Das, 1927; Hughes and Singh, 1971), Ophiocephalus (Das, 1927),
Amia (Neill, 1950), Symbranchus (Johansen, 1966), and the African
and South American lungfishes, Protopterus and Lepidosiren. Ciarlas
and Saccobranchus, another clariid, bury themselves in moist mud
five to six inches below the surface (Das, 1927). But with the
exception of Janssens' (1964) experiments on Protopterus, little is
known of this state.
Most air-breathing fish are facultative air-breathers, employ
ing aquatic breathing unless the water is deoxygenated. Willmer
(1934) observed that high carbon dioxide concentrations also
stimulate air breathing, even when the oxygen content is adequate
for water breathing.
All air-breathing fish utilize aquatic gas exchange to some
extent, because the air-breathing organs show a low gas exchange
ratio. Since carbon dioxide is highly soluble in water, its
elimination takes place primarily through the gills or the skin in
naked forms. Rates of oxygen uptake vary, depending on the
respiratory medium and dominant mode of respiration. Most air
breathers show a reduction in total oxygen consumption when


5
breathing air alone, although this is not the case with obligate
air breathers and forms that are active upon emersion, such as
Periophthalmus.
The morphological and physiological modifications for bimodal
breathing in part account for the ecological success of many of
these species when introduced into new areas. Clarias batrachus, a
clariid catfish that is widely distributed from Ceylon through
eastern India to the Malay Archipelago (Sterba, 1963), was introduced
into the United States for the aquarium trade and escaped from a
"fish farm" near Fort Lauderdale, Florida, probably in 1966 or 1967.
Because of its capacity for air breathing and mobility, £. batrachus
has spread via drainage ditches and canals throughout much of
southeastern Florida.
This study attempts to examine some of the aspects of respiratory
physiology of £. batrachus that have contributed to the success of this
species in south Florida. The breathing response of the animals as
a function of forcible submergence, oxygen tension, time of day,
and body weight was examined. Measurements were made of the rate
of oxygen uptake (VC^) under various experimental conditions
(forcible submergence, air exposure, and water with access to air)
and related to the ecology and behavior of this species. An attempt
was made to determine if £. batrachus utilized anaerobic glycolysis
when the oxygen consumption was reduced during forcible submergence.
Electrocardiograms were taken to compare the cardiac response of
£. batrachus to those of other air breathing fish, and an attempt
was made to induce Clarias to estivate.


6
While this study was in progress, Singh and Hughes (1971)
published results of a similar study of £. batrachus that were
imported from India. Although there was some overlap in the scope
of the two studies, the findings of Singh and Hughes provide valuable
comparative data that augment this study.


MATERIALS AND METHODS
An electro-shocking apparatus and dip nets were used to collect
specimens of £. batrachus in the vicinity of Fort Lauderdale, Florida.
Fish were maintained in aquaria at 25 + 2C on a twelve light/twelve
dark photoperiod.
All metabolic rates were determined at 25 + 1C. Experiments
were conducted during the day to obtain values for resting metabolism,
as Clarias is nocturnal. In a few cases, as during partitioning of
aquatic and aerial phases of respiratory exchange, experiments
continued into the evening. All values for oxygen consumption
were converted to ccC^/kg-hr at STP.
Oxygen uptake of submerged animals was determined through the
use of a chamber (Erlenmeyer flasks or sealed battery jars) from
which samples of water were withdrawn through polyethylene tubing.
A Radiometer PHM 71 Acid-Base Analyzer was used to measure the PO2
of the water sample. Animals were acclimated to the chamber at
least eight hours prior to a determination.
Aerial respiration was determined by manometry. The apparatus
consisted of two equal volume battery jars, serving as the metabolic
and compensation chambers, respectively. A container of Soda Sorb
was placed in the fish chamber to absorb the expired carbon
dioxide. Oxygen used in the metabolic chamber was replaced by
means of a syringe. As long periods of air exposure produced
7


8
skin necrosis, animals were introduced into the chamber for only an
hour before metabolic determinations were made. To determine
cutaneous oxygen uptake in air, a latex condom was placed over the
head of the fish, preventing gas exchange through the air breath
ing organ and gills.
Rates of oxygen uptake in water where the fish had free access
to air were measured in a two section chamber. A small opening
separated the aquatic from the aerial phase. A 1/4 inch mesh
funnel guided the surfacing fish to this opening. Water samples
were drawn from the aquatic chamber for PC^ determinations, and
aerial respiration was determined manometrically. In a control
using water equilibrated with nitrogen there was no significant
amount of diffusion of oxygen into the aquatic phase.
The frequency of aerial breathing as a function of body weight
and time of day and/or amount of incident radiation was determined
with a Hunter Model 3355 photorelay photo cell coupled to an
Esterline Angus event recorder. Air-equilibrated water was
circulated to the recording chamber to keep the PC^ and PCC^
levels constant.
Experiments were conducted to determine whether anaerobic
pathways made a significant contribution to the total energy
expenditure of forcibly submerged animals. Studies of fish
intermediary metabolism (Hochachka, 1969) indicate that the
Embden-Meyerhof pathway is the principal pathway of glucose
catabolism during aerobic metabolism, with the hexose monophosphate
shunt providing a minor contribution, but during anoxia the EMP is


9
operative exclusively. In order to prevent nearly all anaerobic
energy production without greatly interfering with aerobic processes,
fish were injected with iodoacetic acid, which irreversibly inhibits
phosphoglyceraldehyde dehydrogenase and thus blocks the Embden-
Meyerhof pathway prior to any energy release. In one experiment,
fish were injected intraperitoneally with a dosage of 15 mg per kg
of IAA after Belkin (1961). Another group was poisoned with a dosage
of 20 mg per kg, after Rose and Drotman (1967). Half the poisoned fish
(and unaltered controls) were then forcibly submerged in air-equilibrated
water and half were allowed access to air to determine whether such
poisoning was detrimental to submerged fish.
Electrocardiograms were recorded on a Grass Model 79 polygraph.
Two leads were inserted into the fish's body on either side of the
heart and tied dorsally. Fish were anesthetized with MS-222 to
facilitate electrode implantation, and allowed to recover for
. several hours before recordings were made.
Estivation chambers were constructed from a nylon mesh bag
placed inside a hardware cloth frame that was placed inside a
battery jar or refrigerator liner. Mud was placed in the bag, and
the container filled with water. The water was drained off at the
rate of an inch every .other day. Several different mud substrates
% t ;
were used, and in some caces a bright light was left on the fish
during the day.


RESULTS
Ciaras batrachus weighing 69 to 178 g survived at least two
weeks when forcibly submerged in air-saturated water. This species
can also survive out of water for extended periods, provided the
humidity is high and the skin is kept moist. A 54 g individual
survived 3 days and a 124 g individual survived 4 days at 21C when
kept in plastic boxes with wet cheesecloth. Individuals exposed to
room air succumbed in about six to eight hours. The skin of these
individuals rapidly dried during this period.
The rates of oxygen consumption varied greatly as a function
of body weight and access to air. The metabolic rate of forcibly
submerged Ciaras can be described by the relationship Log M =
0.78 Log W 0.82 (r = 0.96; see Fig. 1). Their metabolic rates in
air are described by the relationship Log M = 0.72 Log W 0.54
(r = 0.87; see Fig. 2). When the fish were placed in water and
given access to air their rates of metabolism are described by
the relationship Log M = 0.63 Log W 0.36 (r = 0.93; see Fig. 3).
In Fig. 4 the three curves (forcibly submerged, aerial and water
with access to air) are compared. These curves are essentially
identical in their power of weight, but the curve for forcibly
submerged animals is lower than for individuals that have air
available for gas exchange. The relation of standard energy
metabolism to weight for poikilotherms, corrected to 25C (Log M =
0.75 Log W 0.69, from Hemmingsen, 1960) is also shown in Fig. 4.
10


Figure 1.
Metabolic rate of forcibly submerged JC. batrachus
as a function of body weight.


LOG V02 (cc/hr)
10 100 300


Figure 2.
Metabolic rate of air exposed C
as a function of body weight.
. batrachus


14
IOC 300
10


Figure 3.
Metabolic rate of batrachus, in water with
access to air, as a function of body weight.




Figure 4. Metabolic rates of £. batrachus (forcibly submerged, air
exposed, water with access to air) and poikilotherms (from
Hemmingsen, 1960) as a function of body weight.


LOG V02 (cc/hr)
I f j 1 1 1 1 1 1
10 100 300
00


19
Active metabolism of a few air exposed individuals was obtained;
values for a 220 g and a 113 g individual were 148.2 cc02/kg-hr and
290.2 cc02/kg-hr respectively, as compared to resting rates of
52.5 cc02/kg-hr and 78.5 cc02/kg-hr, respectively (Fig. 2). Activity
then may raise metabolism at least by a factor of three. Cutaneous
respiration accounted for up to 50% of the total oxygen uptake of
two large (200 and 220 g) air exposed fish.
The effects of gradual hypoxia on metabolism of submerged
Clarias weighing 42 to 206 g is shown graphically in Figs. 5, 6, and
7. The metabolic rate appears to be independent of oxygen concen
tration over the range of P02's from saturation to about 40 mmHg.
At oxygen tensions less than 40 mmHg these fish appear to be oxygen
conformers.
As submerged fish exhibited the lowest rates of oxygen uptake,
the question arose whether these fish might depend upon anaerobiosis.
Four fish were poisoned with a 15 mg Iodacetate per kg body weight;
two fish were forcibly submerged in air-saturated water, and the
other two were placed in air-saturated water with access to air. One
unpoisoned fish was placed with each group. Weights of the individuals
used are given below:
Submerged
Access to Air
113 g poisoned
153 g poisoned
178 g normal
156 g poisoned
190 g poisoned
163 g normal
The 153 g individual died after two days, all others survived for
14 days, when the experiment was terminated. This experiment was


Figure 5. Metabolic rate of £. batrachus weighing 42 g as a
function of oxygen tension.




Metabolic rate of C^. batrachus weighing 77 and 83 g
as a function of oxygen tension.
Figure 6.


20 60 100 140 180
WPO2 (mm Hg)
^ ro
co


Figure 7.
Metabolic rate of £. batrachus weighing 172, 195 and
206 g as a function of oxygen tension.


20
100
WPC>2 (mm Hg)
60
140


26
repeated using seven fish and a dosage of 20 mg/kg. The weights
of these fish are given below:
Submerged
77 g poisoned
132 g poisoned
164 g poisoned
180 g poisoned
69 g normal
224 g normal
Access to Air
99 g poisoned
181 g poisoned
139 g poisoned
140 g normal
The 181 g and 139 g individuals, which had access to air went into
tetany when placed in the tank and died in a few hours. The 77 g
individual died during the night. All others survived for two days
and the experiment was terminated. The fact that most of the sub
merged animals that were poisoned survived would tend to preclude
a significant dependence on anaerobiosis when this species is denied
access to air in normoxic water.
The percentage of oxygen uptake from air when the fish were in
water of various 0^ concentrations with access to air is shown in
Figs. 8 and 9. Aquatic breathing accounted for 80% to 90% of the
total oxygen uptake at higher oxygen tensions. At lower oxygen
tensions aerial respiration increases. Smaller fish appear to
increase the amount of aerial respiration at higher oxygen tensions
than larger fish, as the decrease in percentage of aquatic respiration
for smaller fish occurs when oxygen tensions are about 60 mmHg
(Fig. 8) as opposed to 40 mmHg for larger individuals (Fig. 9).
The total oxygen uptake is reduced when Clarias is kept in
deoxygenated water (PO^ = 6 mmHg) with free access to air. The mean
V0o of a 141 g individual was 39.1 cc02/kg-hr compared to a level of


Figure 8. Relationship between oxygen uptake from air and oxygen
tension of the water in C.. batrachus weighing 30-71 g.




Figure 9.
Relationship between oxygen uptake from air and oxygen
tension of the water in £. batrachus weighing 141-210 g.




31
53.5 ccC^/kg-hr in normoxic water. A 71 g individual had a rate
equal to 51.4 ccC^/kg-hr, compared to a normal level of 94.2 ccC^/
kg-hr. Ciaras proved capable of raising the VC>2 under these
conditions; the 71 g fish had an aerial VC^ of 93.8 ccC^/kg-hr
when active in the dark at a water PC^ that averaged 28 mmHg.
This increase was due to increased aerial gas exchange only.
Ciaras can survive for weeks living in oxygen-deficient water if
it has access to air.
The number of air breaths taken per hour is inversely proportional
to the weight of the fish raised to a power less than one and is
influenced by the time of day (and amount of incident radiation)
(Fig. 10). The mean number of daytime surfacings for a 30 g
individual was 19, while that of a 244 g individual was 6. The
surfacing frequency increased by 60% to 100% at night. Lowest
values were between 1100 and 1400 hours EST. On cloudy or rainy
days, surfacings were similar to night values. Any disturbance
(turning on the light at night, standing near the apparatus) caused
surfacing frequency to decline. An 80 g fish place! in nitrogen-
saturated water surfaced about the same number of times during the
day as it did in air-saturated water, but at night the number of
surfacings doubled (see Fig. 11).
Several attempts were made to induce estivation in Ciaras.
Many constructed and used burrows that extended three or four
inches into the mud. Several individuals survived for a period
of three to four days in the estivation chambers, but invariably


Figure 10.
Diurnal and nocturnal surfacing frequency as
function of body weight.


LOG WEIGHT (g)
K3
O
O
ro
O
O
fO Ot
LOG AVERAGE NUMBER OF SURFACINGS/HOUR
ee


Figure 11. Average number of surfacings per hour as a function of time
of day in air-saturated water and nitrogen-saturated water.


AVERAGE NUMBER OF SUR FACINGS/HR.


with the fall in the water level, they emerged, desiccated and
died.
Electrocardiographic measurements of heartbeats demonstrated
some physiological changes upon emersion. Heartbeat frequencies
of a water-breathing fish were around 30 beats/minute and rose to
39 beats/minute following an air breath. When the water was drained
from the tank, bradycardia (15 beats/minute) ensued for about three
minutes, until the fish moved and gulped air. This was followed
by a tachycardia of 78 beats/minute.


DISCUSSION
Ciaras batrachus appears to be a facultative air breather,
as forcibly submerged animals survived at least two weeks. Saxena
(1960) also showed that small C.. batrachus and S^. fossilis could
survive forcible submergence for at least two weeks. Ciaras
batrachus has been described by Singh and Hughes (1971) and Das
(1927) as an obligate air breather. Singh and Hughes (1971)
provided no data to support this supposition, and Das fish
succumbed after two hours when a copper screen was used to prevent
access to the surface. It is possible that copper poisoning, rather
than air deprivation, caused the demise of the fish used in Das'
experiments.
The energy requirements of a fish, which are reflected by the
oxygen consumption, depend on several factors, including physical
properties of the water (amount of oxygen, carbon dioxide, tempera
ture) and the physiological, anatomical, and behavioral modifications
of the fish (ventilation rate, area for gas exchange, activity).
High ventilation rates, large areas for gas exchange, and an oxygen
rich environment all contribute to high rates of oxygen extraction.
Air-breathing fishes, which frequently inhabit waters of low oxygen
tensions, and often show reduced areas for aquatic gas exchange,
might be expected to have low metabolic rates. In Fig. 4, metabolic
curves for C_. batrachus (forcibly submerged, aerial and water with
access to air) are compared to the relation of standard energy
37


38
metabolism to weight for poikilotherms, corrected to 25C (from
Hemmingsen, 1960). The curve for forcibly submerged Clarias is
slightly below the standard poikilotherm curve, while those for
Clarias breathing air or water with access to air are slightly
above.
The metabolic rates of £. batrachus and several other air-
breathing fishes are shown in Table 1. The rates of oxygen
consumption of air-breathing forms are usually labile, depending
upon experimental conditions and are often lowered when the animals
are submerged. In the case of Protopterus and Electrophorus, both
obligate air breathers, the low metabolic rates in submerged animals
are related to their small gill surface area. These fish will
drown if denied access to air.
The lowering of VC^ in submerged Clarias is presumably not due
to the utilization of any anaerobic pathways, as submerged IAA
poisoned fish fared as well as those with access to air. Singh and
Hughes (1971) state that the lowering of the total VC>2 in submerged
Clarias may be related to the reduced surface area of the gills and
the thickness of the gill epithelium. Saxena (1966) found the gill
2
area values of C^. batrachus (295 mm /gm) and of fossilis (395
O
mm^/'gm) were small compared to values of open water forms (Rita rita
2
= 1,000 mm /gm), but when values for Clarias are compared to data
on additional species (Fig. 12, from Muir, 1969), its gill surface
area surpasses those of many purely aquatic breathersthe carp,
Cyprinus carpi; the white sucker, Catostomus commersoni; and the
brown bullhead, Ictalurus nebulosusX Munshi and Singh (1968)


TABLE 1
The Metabolic Rate of Various Air~Breathing Fishes (and Ictalurus
nebulosus) Under Varying Experimental Conditions
Species
Cont. Flow
of Water
Water
& Air
Air
Still
Water
Import, of
Air Breath.
Weight
(gms.)
Temp.
Reference
Anabus
104
testudineus
75.5
113.42
Active
Accessory
29-51
25C
Hughes and Singh, 1970
Anguilla
vulgaris
26.6
11.54
Accessory
475-580
15C
Berg and Steen, 1965
Clarias
batrachus
64.94
93.39
71.17
60.85
Accessory
87-157
25C
Singh and Hughes, 1971
Clarias
batrachus
79.4
79.4
54.9
Accessory
100
25C
Present study
Electrophorus
electricus
29.8
23.04
6.75
Obligate
2,760
26C
Farber and Rahn, 1970
Periophthalmus
sobrinus
94
84
1-5
25C
Gordon et al., 1966
Saccobranchus
fossilis
66.35
84.50
54.50
96.40
Accessory
48-62
25C
Hughes and Singh, 1971
Protopterus
aethiopicus
10
62.5
Obligate
100-600
24C
McMahon, 1970
Sicyuses
sanguinensis
32
40
Accessory
15C
Gordon et al., 1970
Protopterus
aethiopicus
13.5

13.8
Obligate
20C
Lenfant and Johansen, 1968
Ictalurus
nebulosus
70
None
74.9
25C
Marvin and Heath, 1968


Figure 12. Gill surface area as a function of body weight for various
aquatic respiring teleosts (from Muir, 1969) and batrachus
(from Saxena, 1966).
A Mammals
B
Tuna
C
D Most teleosts
E Bass
F Toadfish
G Sucker
H Bullhead
I Clarias


BODY WEIGHT (g.)
TOTAL LAMELLAR AREA (cm.J)


42
determined that the respiratory epithelium is very thick in C_.
batrachus (8 y-15 y as compared to 0.8 y-3.2 y for water breathers).
In addition, they estimated that the thickness of the basement
membrane in £. batrachus precluded all but 52% of the surface area
available for aquatic exchange. Even if Saxena did not account for
the reduction in exposed secondary lamellar area, the proportional
extent of the gill surface of Clarias still exceeds the values of
carp, bullhead, and sucker.
The thickness of the epithelium in Clarias undoubtedly reduces
the rate of diffusion of oxygen into the blood stream. But this is
probably at least partially offset by the high oxygen capacity
(18.0 vol.%, Singh and Hughes, 1971) of the blood. High oxygen
capacity values probably enhance the ability of the blood to pick
up more oxygen while passing through the gills. Johansen et al.
(1968) hypothesized that the high oxygen capacity of Electrophorus
blood was an adaptation to mixing of oxygenated and deoxygenated
blood that results from the shunting of respiratory efferent blood
to the systemic veins. Yet the blood of Symbranchus, Clarias, and
Saccobranchus show the greatest oxygen capacity values (Table 2),
and these species are among the few air-breathing fishes that have
the ideal perfusion pattern (no mixing of arterial and venous
blood) existing in purely aquatic-breathing fishes. All are
facultative air breathers. Symbranchus has a highly reduced gill
2
surface area (40 mm /gm, Junqueiia, Steen and Tinoco, 1967) and the
gill lamellae are thickened so they do not collapse in air. Thus
it may be that the high oxygen capacity enables these primarily


43
TABLE 2
Oxygen Capacities of the Blood of Representative
Air-Breathing Fishes
Species
Clarias batrachus
Saccobranchus fossilis
Electrophorus electricus
Lepidosiren paradoxa
Amia calva
Protopterus aethipicus
Symbranchus marmoratus
Oxygen
Capacity (vol. %)Reference
18.0 Singh and Hughes, 1971
17.5 Singh and Hughes, 1971
13.9 Johansen et al., 1968
8.25 Johansen, 1970.
7.8 Johansen et al., 1970
9.50 Lenfant and Johansen, 1968
17.30 Johansen, 1970


44
aquatic breathers to pick up more oxygen than would normally be
possible through their reduced or thickened gill surfaces. A high
oxygen capacity would also increase the interval between air breaths
when oxygen tensions in water were low, by increasing the oxygen
store of the body.
It appears that the low metabolic rates of submerged animals
are at least partially due to a decrease in activity. Hughes and
Singh (1970) demonstrated that the climbing perch, Anabas testudineus
showed a metabolic rate of 113.4 cc02/kg-hr in water with access to
air, 75.5 cc02/kg-hr while forcibly submerged, but in water with
access to nitrogen, where no additional aerial surface was available
for gas exchange, the VO2 was 127.5 cc02/kg-hr. Thus it appears
that surface area per se is not limiting these animals metabolically
while in the aquatic phase. The surface area available for aquatic
gas exchange certainly must set a limit to the extent of the animal's
activity, but this will be considered later.
Singh and Hughes (1971) report that the mean VO2 of Clarias
in a continuous flow of 50% air saturated water drops to almost
half the value for fully saturated water. If subjected to hypoxia
in a closed chamber, VO2 was reduced from 95.6 cc02/kg-hr at
151 mmHg to 44 cc2/kg-hr at 70 mmHg. These workers further state
that Anabas and Clarias resemble nebulosus and the toadfish
(Opsanus tau) which show oxygen dependent aquatic respiration
(oxygen conformance). The data from the present study demonstrate
that Clarias regulates its oxygen consumption at a constant rate
above water oxygen tensions to about 40 mmHg, suggesting this


45
species is an oxygen regulator. Similarly, Farber and Rahn (1970)
found a linear decrease in water PO2, indicating oxygen regulation,
even at partial pressures as low as 30 mmHg, in the electric eel,
an obligate air breather with reduced gill surface area. Perhaps
Singh and Hughes (1971) were observing a decrease in the active
metabolism of their animals with decreasing PC^ of the water. They
also stated there was no good correlation between weight and weight-
specific oxygen consumption of forcibly submerged fish, which
suggests that some of their animals may have been active.
The critical oxygen tension (Pc)> or partial pressure of
oxygen below which an animal cannot regulate its oxygen consumption,
as a function of body weight is plotted in Fig. 13 for Clarias, a
transitionally breathing aquatic salamander (Siren), and lungless
terrestrial salamanders (Desmognathus). The P£ increases with
increasing body weight for salamanders, and appears to follow the
same relationship in Clarias. Job (1955) found that the effect of
reduced oxygen content on active metabolism was independent of size
for Salvelinus fontinalis, while Beamish (1964) makes no mention
of any effect of size on the level of Pc in the carp and goldfish,
even though he used a weight range of from 17 g-600 g.
Beckenbach (1969) states that the level of P^ depends upon the
weight-specific surface area (and therefore, size) of the animal,
the metabolic rate, and the temperature. The differences in ?c
between terrestrial and aquatic salamanders may be related to the
thickness of the skin, as this is the only gas exchange surface in
these lungless forms, whereas Siren normally utilizes cutaneous,


Figure 13.
Critical oxygen tension of batrachus and
Siren (from Ultsch, 1972) and Desmognathus
1969), as a function of body weight.
two salamanders
(from Beckenbach




48
gill and lung respiration. Ultsch (1971) states that forcibly sub
merged Siren utilize cutaneous respiration almost exclusively. The
cutaneous surface to weight relationships for Siren and Desmognathus
are virtually identical.
The P values of Clarias are about three times lower than those
c
of Siren of a similar weight, even though the metabolic rate of
Clarias is approximately 3.7 times higher (for 100 g animals). The
differences are probably due to the greatly increased surface area
for gas exchange provided by the gills of Clarias.
Singh and Hughes (1971) found that 58.4% of the oxygen uptake
is through the air-breathing organ when the fish were in air-
saturated water with access to air. However, in the present study,
fish that were breathing bimodally in the metabolic chambers did
not surface very often, and little oxygen (10-20% of total) was
taken in through the air-breathing organs. The event recorder data
indicate that the number of surfacings per hour is related to the
weight of the fish, water PO2, time of day, external weather con
ditions, and the amount of disturbance to the fish. As oxygen
consumption values were taken every hour in the metabolic studies,
it is probable that the low values for aerial breathing may be a
result of disturbances that inhibited surfacing. All experiments
were conducted during daylight hours, and, if they extended into
the evening, lighting remained on, a condition which produced low
air-breathing values. In one case (71 g individual), the lights

were turned off for a few hours in the early evening and the VO2
values for aerial breathing doubled. It appears that the gills


49
provide adequate respiratory exchange when the animal is not active,
but increased oxygen uptake for activity is obtained through the
supplemental exchange surface of the air-breathing organ.
Small fish surface more frequently than larger individuals
(Fig. 10) apparently requiring proportionally more oxygen from air
than larger ones. This is unusual for bimodal breathers. McMahon
(1970) found that juvenile lungfish could survive forcible submergence
longer than adults and Ultsch (1972) showed that Siren lacertina, an
aquatic salamander, can function as a water breather at small sizes
only; animals larger than 800 g are obligate air breathers. Although
I did not have any large (300 g or larger) animals, which may be
obligate air breathers, the size range in this study (30-244 g)
indicates that small fish, when given the opportunity, breathe air
more often than large ones.
Saxena (1966) measured the gill surface area of three species
of Indian catfish; one water breather and two air breathers (in
cluding Clarias batrachus). The gill surface area of Rita rita,
a water breather, increases curvilinearly with increasing body
weight as is the usual relationship, while £. batrachus (Fig. 14)
showed no such correlation over a size range of 36-67 g. Perhaps
the proportionally higher metabolic rates coupled with gill surface
areas that are not proportional to weight in small fish account
for the fact that small fish breathe air more often than large
fish.
In oxygen deficient water, where the animals are breathing
air only, the rates of metabolism are minimal, but can be raised


Figure 14. Gill surface area of £. batrachus as a function of
body weight (from Saxena, 1966).


200
1201
30
_JL_
50
60
BODY WEIGHT (9.)
Ln
-u
70
80


52
by increasing the frequency of air breathing. In one case, the
surfacing frequency was measured by event recorder for a fish placed
in nitrogen-saturated water (Fig. 11). The surfacing frequency dur
ing the day was approximately equal to the values for surfacing in
air-saturated water, but the night values were greatly increased.
When the fish are maintained in water with a low oxygen tension,
activity is curtailed (during daylight hours) and they swim slowly
to the surface for a breath, then fall back to the bottom, often
on their sides. Opercular activity is normally diminished or
completely stopped.
Oxygen uptake during air exposure is comparable to values for
fish in water with access to air. Many air-breathing fishes show
reduced VO2 in air, while others (such as the African and South
American lungfishes and electric eel, which are obligate air
breathers, or forms such as Periophthalmus which is active when it
leaves water) show no reduction in Clarias is an example of
the latter case as they are usually active upon emersion. Clarias
is capable of raising the active aerial VO2 to at least three times
the minimal level. The high levels of oxygen uptake in air are
not entirely due to the utilization of the air-breathing organ
because Clarias breathing air in oxygen-deficient water show a 27-46%
decrease in VC^ below values for air-saturated water with access to
air. The skin of these fish may assume up to 50% of the oxygen
uptake in air. Singh and Hughes (1971) found that 16% of the VO2
in air-saturated water was cutaneous. The amount of blood circulating
to the skin evidently increases upon emersion, as the skin of albino


53
individuals becomes pinker and cutaneous VC^ increases. Berg and
Steen (1965) found that cutaneous oxygen uptake of Anguilla vulgaris
is about 2.7 times greater in air than in water. The gills of
Ciaras also probably play an important role in aerial respiration,
as the widely spaced thickened lamellae would not collapse in air
and probably function similarly to those of species that employ
gill breathing in air, such as Symbranchus, Hypopomus and Periopthalmus.
The high aerial VC^ rates of Ciaras batrachus seem somewhat
inconsistent with some of the other aspects of the physiology of
this fish when it is exposed to air. Singh and Hughes (1971)
found that the respiratory quotient of C. batrachus in air was
lower (0.52) than other air-breathing forms they examined (Anabas
and Saccobranchus) even though Anabas is scaled. Howell (1970)
examined the buffering curves of blood of air-breathing fish
(including £. batrachus). These data, plus values for the carp
and bullfrog (from Rahn, 1967), are shown in Fig. 15; all values
are calculated for 25C. Clarias and Neoceratodus, both primarily
water-breathers, have low HCO^ concentrations and are not capable
of buffering blood carbon dioxide much better than the carp. Howell
(1970) states that preliminary laboratory studies indicate that
Clarias goes into severe respiratory acidosis when forced to reside
in air for a few hours. Yet, Clarias is the only one of these air-
breathing fishes that has been reported to leave the water volun
tarily.
The skin of Clarias is very sensitive to desiccation and unless
it is kept moist, a few hours of air exposure produces necrosis of


Figure 15. Buffering capacity of blood of selected
vertebrates at 25C (from Howell, 1970,
and Rahn, 1967).
A Electrophorus
B Rana
C Protopterus
D Lepidosiren
E Cyprinus
F Clarias
G
Neoceratodus


55
PH


56
the skin. Both the sensitivity of the skin and a propensity for
respiratory acidosis in air is probably why Ciaras leaves the water
and migrates mainly (if not exclusively) when it is raining. Ciaras
also follows thin sheets of runoff that flow over roads and down
into the ditches. These conditions maintain a film of water over
the animal's body surface, which prevents skin damage and presumably
would permit carbon dioxide elimination through the naked skin.
In water, Ciaras shows coupling of respiratory and circulatory
adaptations similar to other air-breathing forms such as Electrophorus,
Periophthalmus, and Symbranchus, as maximum cardiac output follows
an air breath. Inflation of the gill chamber in Ciaras corresponds
to an increase in heart rate from about 29 to 39 beats/minute.
Electrocardiograms of Ciaras show physiological features of a
terrestrially active fish such as Periophthalmus. After the
experimental tank was drained, heart rate fell to approximately
half the initial value until the fish moved and took a breath, then
tachycardia ensued with a 250% increase in heart rate. This is
very similar to the results obtained by Johansen (1966) for
Symbranchus. Gordon et al. (1970) found that the Chilean cling-
fish, Sicyases, a fish which is inactive upon emersion, showed an
immediate drop in heart rate upon removal from water. Heart rate
in this fish remained at low levels for the duration of their
emersion.
Clearly, Ciaras batrachus has many characteristics that have
contributed to its success in South Florida. It is able to survive
using aquatic respiration only in aerated water, until the PO2 drops


to very low levels. Air breathing is more common at night, which
tends to decrease susceptibility to predation by diurnally active
predators (herons). When oxygen tensions are low, fish survive by
breathing air and reducing the amount of activity. They can
survive drying (and probably cold in South Florida) by burrowing
in mud or making short excursions to deeper water. During the
rainy season they make extended excursions by water or land to
other waters, which contributes to the dispersal of these species
prior to breeding.


SUMMARY
1. Ciarlas batrachus is a facultative air breather.
2. The V00 of Ciarlas varies as a function of weight and access
to air. The metabolic rates of Ciarlas in air and water with
access to air are essentially the same, but the $C>2 of forcibly
submerged fish is lower.
3. The metabolism characteristic of forcibly submerged Ciarlas
is primarily aerobic, its reduced rate is probably the result
of reduced activity.
4. When the fish are in water with access to air, aquatic breath
ing accounts for 80-90% of the total oxygen uptake. Small
fish appear to increase aerial respiration at higher oxygen
tensions than do large fish.
5. Ciarlas are oxygen regulators at oxygen tensions above 40 mmHg.
6. The critical oxygen tension (Pc) of Ciarlas appears to
increase with increasing body weight, as it does in salamanders.
Because of the increased surface area for gas exchange provided
by the gills of Clarias, the values are about three times
l
lower than those of bimodally-breathing aquatic salamanders
(Siren).
7. The number of air breaths per unit time is a function of time
of day (doubles at night), and is inversely proportional to the
weight of fish. This may be due to the lack of a proportional
58


59
relationship between gill surface area and weight that is shown
in small Clarias (35-68 gms) and also the proportionally
higher metabolic demands of small fish.
8. Oxygen uptake during air exposure is not reduced, as Clarias
is active upon emersion. Cutaneous oxygen uptake accounts for
up to 50% of the total VC^ in air-exposed fish. Cutaneous
vasodilation apparently occurs during emersion.
9. The high oxygen capacity of Clarias blood is probably an
adaptation to facilitate oxygen uptake because of the thickened
and somewhat reduced gill surface area that is necessary for
air breathing and terrestrial activity.
10. Electrocardiographic measurements of heart beat frequencies
demonstrate that Clarias is similar to other air breathers
that are well adapted to emersion.
11. It is suggested that the low HCO^ levels of the blood of
Clarias causing respiratory acidosis after brief periods of
air exposure and the sensitivity of the skin to desiccation
preclude terrestrial activity in Clarias except on rainy
nights when a cutaneous water film (essential for carbon
dioxide exchange) can be maintained.


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BIOGRAPHICAL SKETCH
Jill Ann Jordan was born in Columbia, South Carolina on February 20,
1944. She graduated from Niagara Falls High School in Niagara Falls,
New York and received a Bachelor of Science from Cornell University
in 1966. She received a Master of Science degree from Tulane University
in 1967, and enrolled in the University of Florida. Until the present
time, she has worked toward the Ph.D. in the Department of Zoology.
63


I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
B. K. McNab, Chairman
Professor and Chairman of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
F. G. Nordlie
Associate Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Pierce Brodkorb
Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.


This dissertation was submitted to the Department of Zoology in the
College of Arts and Sciences and to the Graduate Council, and was
accepted as partial fulfillment of the requirements for the degree of
Doctor of Philosophy.
June, 1973
Dean, Graduate School


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PAGE 74

81,9(56,7< 2) )/25,'$


THE INFLUENCE OF BODY WEIGHT ON GAS EXCHANGE IN
THE AIR-BREATHING FISH, Ciarias batrachus
By
JILL ANN JORDAN
A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF
THE UNIVERSITY OF FLORIDA
IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
1973

ACKNOWLEDGEMENTS
I gratefully acknowledge the help of the many people who
contributed to this study. Special thanks go to Vernon Ogilvie
of the Florida Game and Fresh Water Fish Commission who assisted
in collecting specimens and provided much useful information on
the biology of Clarias in Florida, and to Don Goodman who assisted
in collecting, setting up experiments, and proof-reading the manu¬
script.
I am indebted -to Dr. Brian McNab for his assistance and criticisms
and for enduring the clutter and floor-to-ceiling mud in his laboratory,
and to Drs. Frank Nordlie, John Kaufmann, Pierce Brodkorb, Hugh
Popenoe and Stephen Zam for criticism of the manuscript and use of
space and materials. Dr. Gordon Ultsch provided much valuable in¬
formation on the techniques used in the study.
Mr. Paul Laessle provided valuable counsel on the preparation of
the figures, and Ms. Donna Gillis typed the manuscript and aided in
the completion of the final details of preparation.

TABLE OF CONTENTS
Page
Ac knc wl edgements ^
List of Tables iv
List of Figures v
Abstract vii
Introduction 1
Materials and Methods 7
Results 10
Discussion 37
Summary 58
Bibliography 60
Biographical Sketch 63
iii

LIST OF TABLES
Page
1. The Metabolic Rate of Various Air-Breathing Fishes
(and Ictalurus nebulosus) Under Varying
Experimental Conditions 39
2. Oxygen Capacities of the Blood of Representative
Air-Breathing Fishes 43
iv

LIST OF FIGURES
Page
1. Metabolic rate of forcibly submerged £. batrachus
as a function of body weight 12
2. Metabolic rate of air exposed £. batrachus as a
function of body weight 14
3. Metabolic rate of £. batrachus, in water with access
to air, as a function of body weight 16
4. Metabolic rates of £. batrachus (forcibly submerged,
air exposed, water with access to air) and poikilotherms
(from Hemmingsen, 1960) as a function of body weight. ... 18
5. Metabolic rate of £. batrachus weighing 42 g as a
function of oxygen tension 21
6. Metabolic rate of £. batrachus weighing 77 and 83 g
as a function of oxygen tension 23
7. Metabolic rate of £. batrachus weighing 172, 195 and 206 g
as a function of oxygen tension 25
8. Relationship between oxygen uptake from air and oxygen
tension of the water in £. batrachus weighing
30-71 g 28
9. Relationship between oxygen uptake from air and oxygen
tension of the water in £. batrachus weighing
141-210 g 30
10. Diurnal and nocturnal surfacing frequency as a
function of body weight 33
11. Average number of surfacings per hour as a function
of time of day in air-saturated water and nitrogen-
saturated water 35
12. Gill surface area as a function of body weight for
various aquatic respiring teleosts (from Muir, 1969)
and £. batrachus (from Saxena, 1966) 41
v

13. Critical oxygen tension of C_. batrachus and two
salamanders, Siren (from Ultsch, 1972) and
Desmognathus (from Beckenbach, 1969), as a
function of body weight 47
14. Gill surface area of C^. batrachus as a function
of body weight (from Saxena, 1966) 51
15. Buffering capacity of blood of selected vertebrates
at 25°C (from Howell, 1970, and Rahn, 1967) 55
vi

Abstract of Dissertation Presented to the Graduate Council
of the University of Florida in Partial Fulfillment of the Requirements
for the Degree of Doctor of Philosophy
THE INFLUENCE OF BODY WEIGHT ON GAS EXCHANGE IN
THE AIR-BREATHING FISH, Clarias batrachus
By
Jill Ann Jordan
June, 1973
Chairman: Dr. B. K. McNab
Major Department: Zoology
Aerial respiration and its capacity for terrestrial locomotion
have enabled Clarias batrachus, a clariid catfish from southern
Asia, to establish a large breeding population in southeastern
Florida. Clarias batrachus is a facultative air breather, and at
aquatic oxygen tensions exceeding 40 mmHg, an oxygen regulator.
The rate of metabolism of Clarias varies as a function of
weight, and access to air. Aerobic metabolism is primarily utilized,
even during forcible submergence when the metabolic rate declines.
Clarias, a terrestrially active fish under certain environmental
conditions, shows no metabolic reduction upon emersion.
The aquatic oxygen tension below which Clarias becomes an
oxygen conformer is directly proportional to body weight, and about
1/3 the value for bimodally breathing salamanders; the disparity is
presumably the result of the greater surface area for gaseous exchange
in Clarias.
The number of air breaths per unit time doubles at night and
is inversely proportional to body weight.
vii

The sensitivity of its naked skin to desiccation and the low
bicarbonate buffering capacity of its blood limit the terrestrial
activity of Clarias to rainy nights when a cutaneous film of water
can be maintained.
viii

INTRODUCTION
The transition from aquatic to aerial breathing was one of the
most important events in vertebrate evolution. Air breathing has
evolved in numerous taxonomically unrelated groups of teleosts, and
has produced a remarkable degree of convergence in these fishes.
Bimodal breathers run the respiratory gamut from facultative air
breathers that can survive indefinitely on the oxygen dissolved in
water (except in times of severe oxygen stress), to obligate air
breathers (such as Electrophorus, Lepidosiren, and Protopterus)
that will drown when denied access to air; hence this is an excellent
group in which to study the physiological modifications imposed by
bimodal respiration. One such bimodally breathing teleost, Clarias
batrachus, the "walking catfish," is the subject of this study.
Air breathing has enabled this exotic introduction from southern
Asia to become one of the dominant fishes in southeastern Florida;
hence this species is an interesting form in which to study some
of the aspects of bimodal respiration that have contributed to
its success.
The two respiratory media, water and air, differ greatly in
their physical properties, imposing very different morphological
and physiological adaptations on the structure and function of
respiratory surfaces. Water is a medium that often offers marginal
conditions for gas exchange. It is frequently oxygen deficient.
At 25°C, oxygen attains only 1/35 the concentration in water that
1

2
it does in air, but carbon dioxide is 27 times more soluble in water
than oxygen, and may reach concentrations greatly in excess of
aerial values. Consequently water breathers must ventilate much
larger volumes of a denser medium than air breathers for a similar
oxygen uptake. Air, In contrast, with its high partial pressure
of oxygen offers a favorable diffusion gradient but requires
significant structural support for respiratory surfaces. Furthermore,
an atmospheric humidity below saturation will cause evaporation from
the epithelial surfaces that must remain moist for gas exchange.
Therefore a premium is placed upon structures protected within the
body for aerial gas exchange. Obligate air breathers also must have
an increased efficiency of the internal buffering system because of
the elevated internal carbon dioxide tensions.
Since the differences in gaseous composition between air
and water increase with temperature, it is not surprising that
the majority of extant air-breathing fishes live in tropical fresh-
waters. These relatively warm waters usually have low oxygen and
high carbon dioxide concentrations, due to the lack of turnover
(because there is little wind disturbance and night temperatures
are not cool enough), the reduction of aquatic photosynthetic
activity because of shading, and the high B.O.D. of such waters.
Only a few temperate fresh-water species exhibit air breathing
(Lepisosteus, Amia, and Umbra). Johansen (1970) demonstrated that
air breathing in Amia calva increases at higher temperatures. The
few marine air-breathing fish [some members of the families
Gobiidae (including the mud skippers) and Blennidae, the clingfish
I

3
Sicyases (Gordon et al., 1970), the eel, Anguilla (Berg and Steen,
1965), and tarpons (Elopidae)] are mostly estuarine $>ecies and
probably often encounter deoxygenated water in areas of organic
decomposition such as mud flats, mangroves and vegetation mats.
i • ■
Air breathing has enabled many of these fish to not only
inhabit water with unfavorable gas tensions, but even to leave the
water and spend part of their time on land. Certain fish, such as
Anguilla (Berg and Steen, 1965), Symbranchus (Johansen, 1966),
Ciarlas batrachus (Smith, 1945; Das, 1927), Saccobranchus "
Heteropneustes, Anabas and Ophiocephalus (Das, 1927), frequently
make night sojourns from pond to pond through moist grass. Some
of these fishes are thought to feed while making these excursions.
The Chilean clingfish, Sicyases sanguinensis (Gordon et al., 1970)
rests on rocks in the inter-tidal splash zone, while the more
active mudskipper, Periophthalmus, actually leaves the water to
escape predators and to feed (Johansen, 1970). Other fish, such
as African species of Ciarlas may move from drying pools to permanent
bodies of water. Desiccation is a problem faced by most of these
fish when they leave the water, hence the extent of these land
excursions is a function of weather conditions, time of day,
and physical conditions of the area.
In India (Das, 1927) and in south Florida (Ogilvie, personal
communication), great numbers of Ciarlas batrachus migrate in the
rainy season, presumably for feeding purposes. Mookerjee and
Mazumdar (1950) reported that Ciarlas batrachus rarely migrates

4
by a land route like Anabas, but frequently migrates in shallow
running water. This account corroborates descriptions of its
behavior in south Florida, and some of the conclusions reached in
this study.
If they are unable to escape a drying pool, certain air-breath¬
ing fish burrow into the mud and become dormant. Estivation has been
reported for Ciarías (Das, 1927; Sterba, 1963), Saccobranchus
(Das, 1927; Hughes and Singh, 1971), Ophiocephalus (Das, 1927),
Amia (Neill, 1950), Symbranchus (Johansen, 1966), and the African
and South American lungfishes, Protopterus and Lepidosiren. Ciarlas
and Saccobranchus, another clariid, bury themselves in moist mud
five to six inches below the surface (Das, 1927). But with the
exception of Janssens' (1964) experiments on Protopterus, little is
known of this state.
Most air-breathing fish are facultative air-breathers, employ¬
ing aquatic breathing unless the water is deoxygenated. Willmer
(1934) observed that high carbon dioxide concentrations also
stimulate air breathing, even when the oxygen content is adequate
for water breathing.
All air-breathing fish utilize aquatic gas exchange to some
extent, because the air-breathing organs show a low gas exchange
ratio. Since carbon dioxide is highly soluble in water, its
elimination takes place primarily through the gills or the skin in
naked forms. Rates of oxygen uptake vary, depending on the
respiratory medium and dominant mode of respiration. Most air
breathers show a reduction in total oxygen consumption when

5
breathing air alone, although this is not the case with obligate
air breathers and forms that are active upon emersion, such as
Periophthalmus.
The morphological and physiological modifications for bimodal
breathing in part account for the ecological success of many of
these species when introduced into new areas. Clarias batrachus, a
clariid catfish that is widely distributed from Ceylon through
eastern India to the Malay Archipelago (Sterba, 1963), was introduced
into the United States for the aquarium trade and escaped from a
"fish farm" near Fort Lauderdale, Florida, probably in 1966 or 1967.
Because of its capacity for air breathing and mobility, £. batrachus
has spread via drainage ditches and canals throughout much of
southeastern Florida.
This study attempts to examine some of the aspects of respiratory
physiology of £. batrachus that have contributed to the success of this
species in south Florida. The breathing response of the animals as
a function of forcible submergence, oxygen tension, time of day,
and body weight was examined. Measurements were made of the rate
of oxygen uptake (VC^) under various experimental conditions
(forcible submergence, air exposure, and water with access to air)
and related to the ecology and behavior of this species. An attempt
was made to determine if £. batrachus utilized anaerobic glycolysis
when the oxygen consumption was reduced during forcible submergence.
Electrocardiograms were taken to compare the cardiac response of
£. batrachus to those of other air breathing fish, and an attempt
was made to induce Clarias to estivate.

6
While this study was in progress, Singh and Hughes (1971)
published results of a similar study of £. batrachus that were
imported from India. Although there was some overlap in the scope
of the two studies, the findings of Singh and Hughes provide valuable
comparative data that augment this study.

MATERIALS AND METHODS
An electro-shocking apparatus and dip nets were used to collect
specimens of £. batrachus in the vicinity of Fort Lauderdale, Florida.
Fish were maintained in aquaria at 25 + 2°C on a twelve light/twelve
dark photoperiod.
All metabolic rates were determined at 25 + 1°C. Experiments
were conducted during the day to obtain values for resting metabolism,
as Ciarías is nocturnal. In a few cases, as during partitioning of
aquatic and aerial phases of respiratory exchange, experiments
continued into the evening. All values for oxygen consumption
were converted to ccC^/kg-hr at STP.
Oxygen uptake of submerged animals was determined through the
use of a chamber (Erlenmeyer flasks or sealed battery jars) from
which samples of water were withdrawn through polyethylene tubing.
A Radiometer PHM 71 Acid-Base Analyzer was used to measure the PO2
of the water sample. Animals were acclimated to the chamber at
least eight hours prior to a determination.
Aerial respiration was determined by manometry. The apparatus
consisted of two equal volume battery jars, serving as the metabolic
and compensation chambers, respectively. A container of Soda Sorb
was placed in the fish chamber to absorb the expired carbon
dioxide. Oxygen used in the metabolic chamber was replaced by
means of a syringe. As long periods of air exposure produced
7

8
skin necrosis, animals were introduced into the chamber for only an
hour before metabolic determinations were made. To determine
cutaneous oxygen uptake in air, a latex condom was placed over the
head of the fish, preventing gas exchange through the air breath¬
ing organ and gills.
Rates of oxygen uptake in water where the fish had free access
to air were measured in a two section chamber. A small opening
separated the aquatic from the aerial phase. A 1/4 inch mesh
funnel guided the surfacing fish to this opening. Water samples
were drawn from the aquatic chamber for PC^ determinations, and
aerial respiration was determined manometrically. In a control
using water equilibrated with nitrogen there was no significant
amount of diffusion of oxygen into the aquatic phase.
The frequency of aerial breathing as a function of body weight
and time of day and/or amount of incident radiation was determined
with a Hunter Model 3355 photorelay photo cell coupled to an
Esterline Angus event recorder. Air-equilibrated water was
circulated to the recording chamber to keep the PC^ and PCC^
levels constant.
Experiments were conducted to determine whether anaerobic
pathways made a significant contribution to the total energy
expenditure of forcibly submerged animals. Studies of fish
intermediary metabolism (Hochachka, 1969) indicate that the
Embden-Meyerhof pathway is the principal pathway of glucose
catabolism during aerobic metabolism, with the hexose monophosphate
shunt providing a minor contribution, but during anoxia the EMP is

9
operative exclusively. In order to prevent nearly all anaerobic
energy production without greatly interfering with aerobic processes,
fish were injected with iodoacetic acid, which irreversibly inhibits
phosphoglyceraldehyde dehydrogenase and thus blocks the Embden-
Meyerhof pathway prior to any energy release. In one experiment,
fish were injected intraperitoneally with a dosage of 15 mg per kg
of IAA after Belkin (1961). Another group was poisoned with a dosage
of 20 mg per kg, after Rose and Drotman (1967). Half the poisoned fish
(and unaltered controls) were then forcibly submerged in air-equilibrated
water and half were allowed access to air to determine whether such
poisoning was detrimental to submerged fish.
Electrocardiograms were recorded on a Grass Model 79 polygraph.
Two leads were inserted into the fish's body on either side of the
heart and tied dorsally. Fish were anesthetized with MS-222 to
facilitate electrode implantation, and allowed to recover for
. several hours before recordings were made.
Estivation chambers were constructed from a nylon mesh bag
placed inside a hardware cloth frame that was placed inside a
battery jar or refrigerator liner. Mud was placed in the bag, and
the container filled with water. The water was drained off at the
rate of an inch every .other day. Several different mud substrates
were used, and in some caces a bright light was left on the fish
during the day.

RESULTS
Ciarías batrachus weighing 69 to 178 g survived at least two
weeks when forcibly submerged in air-saturated water. This species
can also survive out of water for extended periods, provided the
humidity is high and the skin is kept moist. A 54 g individual
survived 3 days and a 124 g individual survived 4 days at 21°C when
kept in plastic boxes with wet cheesecloth. Individuals exposed to
room air succumbed in about six to eight hours. The skin of these
individuals rapidly dried during this period.
The rates of oxygen consumption varied greatly as a function
of body weight and access to air. The metabolic rate of forcibly
submerged Clarias can be described by the relationship Log M =
0.78 Log W - 0.82 (r = 0.96; see Fig. 1). Their metabolic rates in
air are described by the relationship Log M = 0.72 Log W - 0.54
(r = 0.87; see Fig. 2). When the fish were placed in water and
given access to air their rates of metabolism are described by
the relationship Log M = 0.63 Log W - 0.36 (r = 0.93; see Fig. 3).
In Fig. 4 the three curves (forcibly submerged, aerial and water
with access to air) are compared. These curves are essentially
identical in their power of weight, but the curve for forcibly
submerged animals is lower than for individuals that have air
available for gas exchange. The relation of standard energy
metabolism to weight for poikilotherms, corrected to 25°C (Log M =
0.75 Log W - 0.69, from Hemmingsen, 1960) is also shown in Fig. 4.
10

Figure 1.
Metabolic rate of forcibly submerged JC. batrachus
as a function of body weight.

LOG V02 (cc/hr)
10 100 300

Figure 2.
Metabolic rate of air
as a function of body
exposed C_. batrachus
weight.

14
IOC 300
10

Figure 3.
Metabolic rate of batrachus, in water with
access to air, as a function of body weight.


Figure 4. Metabolic rates of £. batrachus (forcibly submerged, air
exposed, water with access to air) and poikilotherms (from
Hemmingsen, 1960) as a function of body weight.

LOG V02 (cc/hr)
I f j 1 1 1 1 1 1—
10 100 300
00

19
Active metabolism of a few air exposed individuals was obtained;
values for a 220 g and a 113 g individual were 148.2 cc02/kg-hr and
290.2 cc02/kg-hr respectively, as compared to resting rates of
52.5 cc02/kg-hr and 78.5 cc02/kg-hr, respectively (Fig. 2). Activity
then may raise metabolism at least by a factor of three. Cutaneous
respiration accounted for up to 50% of the total oxygen uptake of
two large (200 and 220 g) air exposed fish.
The effects of gradual hypoxia on metabolism of submerged
Clarias weighing 42 to 206 g is shown graphically in Figs. 5, 6, and
7. The metabolic rate appears to be independent of oxygen concen¬
tration over the range of P02's from saturation to about 40 mmHg.
At oxygen tensions less than 40 mmHg these fish appear to be oxygen
conformers.
As submerged fish exhibited the lowest rates of oxygen uptake,
the question arose whether these fish might depend upon anaerobiosis.
Four fish were poisoned with a 15 mg Iodacetate per kg body weight;
two fish were forcibly submerged in air-saturated water, and the
other two were placed in air-saturated water with access to air. One
unpoisoned fish was placed with each group. Weights of the individuals
used are given below:
Submerged
Access to Air
113 g poisoned
153 g poisoned
178 g normal
156 g poisoned
190 g poisoned
163 g normal
The 153 g individual died after two days, all others survived for
14 days, when the experiment was terminated. This experiment was

Figure 5. Metabolic rate of £. batrachus weighing 42 g as a
function of oxygen tension.


Metabolic rate of C^. batrachus weighing 77 and 83 g
as a function of oxygen tension.
Figure 6.

20 60 100 140 180
WPO2 (mm Hg)
^ ro
lo

Figure 7.
Metabolic rate of £. batrachus weighing 172, 195 and
206 g as a function of oxygen tension.

20
100
WPC>2 (mm Hg)
60
140

26
repeated using seven fish and a dosage of 20 mg/kg. The weights
of these fish are given below:
Submerged
77 g poisoned
132 g poisoned
164 g poisoned
180 g poisoned
69 g normal
224 g normal
Access to Air
99 g poisoned
181 g poisoned
139 g poisoned
140 g normal
The 181 g and 139 g individuals, which had access to air went into
tetany when placed in the tank and died in a few hours. The 77 g
individual died during the night. All others survived for two days
and the experiment was terminated. The fact that most of the sub¬
merged animals that were poisoned survived would tend to preclude
a significant dependence on anaerobiosis when this species is denied
access to air in normoxic water.
The percentage of oxygen uptake from air when the fish were in
water of various 0^ concentrations with access to air is shown in
Figs. 8 and 9. Aquatic breathing accounted for 80% to 90% of the
total oxygen uptake at higher oxygen tensions. At lower oxygen
tensions aerial respiration increases. Smaller fish appear to
increase the amount of aerial respiration at higher oxygen tensions
than larger fish, as the decrease in percentage of aquatic respiration
for smaller fish occurs when oxygen tensions are about 60 mmHg
(Fig. 8) as opposed to 40 mmHg for larger individuals (Fig. 9).
The total oxygen uptake is reduced when Clarias is kept in
deoxygenated water (PO^ = 6 mmHg) with free access to air. The mean
V0o of a 141 g individual was 39.1 cc02/kg-hr compared to a level of

Figure 8. Relationship between oxygen uptake from air and oxygen
tension of the water in C.. batrachus weighing 30-71 g.


Figure 9.
Relationship between oxygen uptake from air and oxygen
tension of the water in £. batrachus weighing 141-210 g.


31
53.5 ccC^/kg-hr in normoxic water. A 71 g individual had a rate
equal to 51.4 ccC^/kg-hr, compared to a normal level of 94.2 ccC^/
kg-hr. Ciarías proved capable of raising the VC>2 under these
conditions; the 71 g fish had an aerial VC^ of 93.8 ccC^/kg-hr
when active in the dark at a water PC^ that averaged 28 mmHg.
This increase was due to increased aerial gas exchange only.
Clarias can survive for weeks living in oxygen-deficient water if
it has access to air.
The number of air breaths taken per hour is inversely proportional
to the weight of the fish raised to a power less than one and is
influenced by the time of day (and amount of incident radiation)
(Fig. 10). The mean number of daytime surfacings for a 30 g
individual was 19, while that of a 244 g individual was 6. The
surfacing frequency increased by 60% to 100% at night. Lowest
values were between 1100 and 1400 hours EST. On cloudy or rainy
days, surfacings were similar to night values. Any disturbance
(turning on the light at night, standing near the apparatus) caused
surfacing frequency to decline. An 80 g fish placel in nitrogen-
saturated water surfaced about the same number of times during the
day as it did in air-saturated water, but at night the number of
surfacings doubled (see Fig. 11).
Several attempts were made to induce estivation in Clarias.
Many constructed and used burrows that extended three or four
inches into the mud. Several individuals survived for a period
of three to four days in the estivation chambers, but invariably

Figure 10.
Diurnal and nocturnal surfacing frequency as
function of body weight.

LOG WEIGHT (g)
K3
O
O
ro
O
O
fO Ot
LOG AVERAGE NUMBER OF SURFACINGS/HOUR
ee

Figure 11. Average number of surfacings per hour as a function of time
of day in air-saturated water and nitrogen-saturated water.

AVERAGE NUMBER OF SUR FACINGS/HR.

with the fall in the water level, they emerged, desiccated and
died.
Electrocardiographic measurements of heartbeats demonstrated
some physiological changes upon emersion. Heartbeat frequencies
of a water-breathing fish were around 30 beats/minute and rose to
39 beats/minute following an air breath. When the water was drained
from the tank, bradycardia (15 beats/minute) ensued for about three
minutes, until the fish moved and gulped air. This was followed
by a tachycardia of 78 beats/minute.

DISCUSSION
Ciarías batrachus appears to be a facultative air breather,
as forcibly submerged animals survived at least two weeks. Saxena
(1960) also showed that small C.. batrachus and j5. fossilis could
survive forcible submergence for at least two weeks. Ciarías
batrachus has been described by Singh and Hughes (1971) and Das
(1927) as an obligate air breather. Singh and Hughes (1971)
provided no data to support this supposition, and Das’ fish
succumbed after two hours when a copper screen was used to prevent
access to the surface. It is possible that copper poisoning, rather
than air deprivation, caused the demise of the fish used in Das'
experiments.
The energy requirements of a fish, which are reflected by the
oxygen consumption, depend on several factors, including physical
properties of the water (amount of oxygen, carbon dioxide, tempera¬
ture) and the physiological, anatomical, and behavioral modifications
of the fish (ventilation rate, area for gas exchange, activity).
High ventilation rates, large areas for gas exchange, and an oxygen
rich environment all contribute to high rates of oxygen extraction.
Air-breathing fishes, which frequently inhabit waters of low oxygen
tensions, and often show reduced areas for aquatic gas exchange,
might be expected to have low metabolic rates. In Fig. 4, metabolic
curves for C^. batrachus (forcibly submerged, aerial and water with
access to air) are compared to the relation of standard energy
37

38
metabolism to weight for poikilotherms, corrected to 25°C (from
Hemmingsen, 1960). The curve for forcibly submerged Clarias is
slightly below the standard poikilotherm curve, while those for
Clarias breathing air or water with access to air are slightly
above.
The metabolic rates of £. batrachus and several other air-
breathing fishes are shown in Table 1. The rates of oxygen
consumption of air-breathing forms are usually labile, depending
upon experimental conditions and are often lowered when the animals
are submerged. In the case of Protopterus and Electrophorus, both
obligate air breathers, the low metabolic rates in submerged animals
are related to their small gill surface area. These fish will
drown if denied access to air.
The lowering of VC^ in submerged Clarias is presumably not due
to the utilization of any anaerobic pathways, as submerged IAA
poisoned fish fared as well as those with access to air. Singh and
Hughes (1971) state that the lowering of the total VC^ in submerged
Clarias may be related to the reduced surface area of the gills and
the thickness of the gill epithelium. Saxena (1966) found the gill
2
area values of C^. batrachus (295 mm /gm) and of fossilis (395
O
mm^/'gm) were small compared to values of open water forms (Rita rita
2
= 1,000 mm /gm), but when values for Clarias are compared to data
on additional species (Fig. 12, from Muir, 1969), its gill surface
area surpasses those of many purely aquatic breathers—the carp,
Cyprinus carpió; the white sucker, Catostomus commersoni; and the
brown bullhead, Ictalurus nebulosusX Munshi and Singh (1968)

TABLE 1
The Metabolic Rate of Various Air~Breathing Fishes (and Ictalurus
nebulosus) Under Varying Experimental Conditions
Species
Cont. Flow
of Water
Water
& Air
Air
Still
Water
Import, of
Air Breath.
Weight
(gms.)
Temp.
Reference
Anabus
104
testudineus
75.5
113.42
Active
Accessory
29-51
25°C
Hughes and Singh, 1970
Anguilla
vulgaris
26.6
11.54
Accessory
475-580
15°C
Berg and Steen, 1965
Clarias
batrachus
64.94
93.39
71.17
60.85
Accessory
87-157
25°C
Singh and Hughes, 1971
Clarias
batrachus
79.4
79.4
54.9
Accessory
100
25°C
Present study
Electrophorus
electricus
29.8
23.04
6.75
Obligate
2,760
26°C
Farber and Rahn, 1970
Periophthalmus
sobrinus
94
84
1-5
25°C
Gordon et al., 1966
Saccobranchus
fossilis
66.35
84.50
54.50
96.40
Accessory
48-62
25°C
Hughes and Singh, 1971
Protopterus
aethiopicus
10
62.5
Obligate
100-600
24°C
McMahon, 1970
Sicyuses
sanguinensis
32
40
Accessory
15°C
Gordon et al., 1970
Protopterus
aethiopicus
13.5
%
13.8
Obligate
20°C
Lenfant and Johansen, 1968
Ictalurus
'
nebulosus
70
None
74.9
25°C
Marvin and Heath, 1968

Figure 12. Gill surface area as a function of body weight for various
aquatic respiring teleosts (from Muir, 1969) and batrachus
(from Saxena, 1966).
A Mammals
B
Tuna
C
D Most teleosts
E Bass
F Toadfish
G Sucker
H Bullhead
I Clarias

BODY WEIGHT (g.)
TOTAL LAMELLAR AREA (cm.J)

42
determined that the respiratory epithelium is very thick in C_.
batrachus (8 y-15 y as compared to 0.8 y-3.2 y for water breathers).
In addition, they estimated that the thickness of the basement
membrane in £. batrachus precluded all but 52% of the surface area
available for aquatic exchange. Even if Saxena did not account for
the reduction in exposed secondary lamellar area, the proportional
extent of the gill surface of Clarias still exceeds the values of
carp, bullhead, and sucker.
The thickness of the epithelium in Clarias undoubtedly reduces
the rate of diffusion of oxygen into the blood stream. But this is
probably at least partially offset by the high oxygen capacity
(18.0 vol.%, Singh and Hughes, 1971) of the blood. High oxygen
capacity values probably enhance the ability of the blood to pick
up more oxygen while passing through the gills. Johansen et al.
(1968) hypothesized that the high oxygen capacity of Electrophorus
blood was an adaptation to mixing of oxygenated and deoxygenated
blood that results from the shunting of respiratory efferent blood
to the systemic veins. Yet the blood of Symbranchus, Clarias, and
Saccobranchus show the greatest oxygen capacity values (Table 2),
and these species are among the few air-breathing fishes that have
the ideal perfusion pattern (no mixing of arterial and venous
blood) existing in purely aquatic-breathing fishes. All are
facultative air breathers. Symbranchus has a highly reduced gill
surface area (40 mm /gm, Junqueiia, Steen and Tinoco, 1967) and the
gill lamellae are thickened so they do not collapse in air. Thus
it may be that the high oxygen capacity enables these primarily

43
TABLE 2
Oxygen Capacities of the Blood of Representative
Air-Breathing Fishes
Species
Clarias batrachus
Saccobranchus fossilis
Electrophorus electricus
Lepidosiren paradoxa
Amia calva
Protopterus aethipicus
Symbranchus marmoratus
Oxygen
Capacity (vol. %)Reference
18.0 Singh and Hughes, 1971
17.5 Singh and Hughes, 1971
13.9 Johansen et al., 1968
8.25 Johansen, 1970.
7.8 Johansen et al., 1970
9.50 Lenfant and Johansen, 1968
17.30 Johansen, 1970

44
aquatic breathers to pick up more oxygen than would normally be
possible through their reduced or thickened gill surfaces. A high
oxygen capacity would also increase the interval between air breaths
when oxygen tensions in water were low, by increasing the oxygen
store of the body.
It appears that the low metabolic rates of submerged animals
are at least partially due to a decrease in activity. Hughes and
Singh (1970) demonstrated that the climbing perch, Anabas testudineus
showed a metabolic rate of 113.4 cc02/kg-hr in water with access to
air, 75.5 cc02/kg-hr while forcibly submerged, but in water with
access to nitrogen, where no additional aerial surface was available
for gas exchange, the VO2 was 127.5 cc02/kg-hr. Thus it appears
that surface area per se is not limiting these animals metabolically
while in the aquatic phase. The surface area available for aquatic
gas exchange certainly must set a limit to the extent of the animal's
activity, but this will be considered later.
Singh and Hughes (1971) report that the mean VO2 of Clarias
in a continuous flow of 50% air saturated water drops to almost
half the value for fully saturated water. If subjected to hypoxia
in a closed chamber, VO2 was reduced from 95.6 cc02/kg-hr at
151 mmHg to 44 cc02/kg-hr at 70 mmHg. These workers further state
that Anabas and Clarias resemble nebulosus and the toadfish
(Opsanus tau) which show oxygen dependent aquatic respiration
(oxygen conformance). The data from the present study demonstrate
that Clarias regulates its oxygen consumption at a constant rate
above water oxygen tensions to about 40 mmHg, suggesting this

45
species is an oxygen regulator. Similarly, Farber and Rahn (1970)
found a linear decrease in water PO2, indicating oxygen regulation,
even at partial pressures as low as 30 mmHg, in the electric eel,
an obligate air breather with reduced gill surface area. Perhaps
Singh and Hughes (1971) were observing a decrease in the active
metabolism of their animals with decreasing PC^ of the water. They
also stated there was no good correlation between weight and weight-
specific oxygen consumption of forcibly submerged fish, which
suggests that some of their animals may have been active.
The critical oxygen tension (Pc)> or partial pressure of
oxygen below which an animal cannot regulate its oxygen consumption,
as a function of body weight is plotted in Fig. 13 for Clarias, a
transitionally breathing aquatic salamander (Siren), and lungless
terrestrial salamanders (Desmognathus). The P£ increases with
increasing body weight for salamanders, and appears to follow the
same relationship in Clarias. Job (1955) found that the effect of
reduced oxygen content on active metabolism was independent of size
for Salvelinus fontinalis, while Beamish (1964) makes no mention
of any effect of size on the level of Pc in the carp and goldfish,
even though he used a weight range of from 17 g-600 g.
Beckenbach (1969) states that the level of P^ depends upon the
weight-specific surface area (and therefore, size) of the animal,
the metabolic rate, and the temperature. The differences in ?c
between terrestrial and aquatic salamanders may be related to the
thickness of the skin, as this is the only gas exchange surface in
these lungless forms, whereas Siren normally utilizes cutaneous,

Figure 13.
Critical oxygen tension of batrachus and
Siren (from Ultsch, 1972) and Desmognathus
1969), as a function of body weight.
two salamanders
(from Beckenbach


48
gill and lung respiration. Ultsch (1971) states that forcibly sub¬
merged Siren utilize cutaneous respiration almost exclusively. The
cutaneous surface to weight relationships for Siren and Desmognathus
are virtually identical.
The P values of Clarias are about three times lower than those
c
of Siren of a similar weight, even though the metabolic rate of
Clarias is approximately 3.7 times higher (for 100 g animals). The
differences are probably due to the greatly increased surface area
for gas exchange provided by the gills of Clarias.
Singh and Hughes (1971) found that 58.4% of the oxygen uptake
is through the air-breathing organ when the fish were in air-
saturated water with access to air. However, in the present study,
fish that were breathing bimodally in the metabolic chambers did
not surface very often, and little oxygen (10-20% of total) was
taken in through the air-breathing organs. The event recorder data
indicate that the number of surfacings per hour is related to the
weight of the fish, water PO2, time of day, external weather con¬
ditions, and the amount of disturbance to the fish. As oxygen
consumption values were taken every hour in the metabolic studies,
it is probable that the low values for aerial breathing may be a
result of disturbances that inhibited surfacing. All experiments
were conducted during daylight hours, and, if they extended into
the evening, lighting remained on, a condition which produced low
air-breathing values. In one case (71 g individual), the lights
•
were turned off for a few hours in the early evening and the VO2
values for aerial breathing doubled. It appears that the gills

49
provide adequate respiratory exchange when the animal is not active,
but increased oxygen uptake for activity is obtained through the
supplemental exchange surface of the air-breathing organ.
Small fish surface more frequently than larger individuals
(Fig. 10) apparently requiring proportionally more oxygen from air
than larger ones. This is unusual for bimodal breathers. McMahon
(1970) found that juvenile lungfish could survive forcible submergence
longer than adults and Ultsch (1972) showed that Siren lacertina, an
aquatic salamander, can function as a water breather at small sizes
only; animals larger than 800 g are obligate air breathers. Although
I did not have any large (300 g or larger) animals, which may be
obligate air breathers, the size range in this study (30-244 g)
indicates that small fish, when given the opportunity, breathe air
more often than large ones.
Saxena (1966) measured the gill surface area of three species
of Indian catfish; one water breather and two air breathers (in¬
cluding Clarias batrachus). The gill surface area of Rita rita,
a water breather, increases curvilinearly with increasing body
weight as is the usual relationship, while £. batrachus (Fig. 14)
showed no such correlation over a size range of 36-67 g. Perhaps
the proportionally higher metabolic rates coupled with gill surface
areas that are not proportional to weight in small fish account
for the fact that small fish breathe air more often than large
fish.
In oxygen deficient water, where the animals are breathing
air only, the rates of metabolism are minimal, but can be raised

Figure 14. Gill surface area of £. batrachus as a function of
body weight (from Saxena, 1966).

200
CN
É
u
<
LU
cm
<
o
§
180
160
140-
120
30
40
_JL_
50
60
BODY WEIGHT (9.)
Ln
-u
70
80

52
by increasing the frequency of air breathing. In one case, the
surfacing frequency was measured by event recorder for a fish placed
in nitrogen-saturated water (Fig. 11). The surfacing frequency dur¬
ing the day was approximately equal to the values for surfacing in
air-saturated water, but the night values were greatly increased.
When the fish are maintained in water with a low oxygen tension,
activity is curtailed (during daylight hours) and they swim slowly
to the surface for a breath, then fall back to the bottom, often
on their sides. Opercular activity is normally diminished or
completely stopped.
Oxygen uptake during air exposure is comparable to values for
fish in water with access to air. Many air-breathing fishes show
reduced VO2 in air, while others (such as the African and South
American lungfishes and electric eel, which are obligate air
breathers, or forms such as Periophthalmus which is active when it
leaves water) show no reduction in Clarias is an example of
the latter case as they are usually active upon emersion. Clarias
is capable of raising the active aerial VO2 to at least three times
the minimal level. The high levels of oxygen uptake in air are
not entirely due to the utilization of the air-breathing organ
because Clarias breathing air in oxygen-deficient water show a 27-46%
decrease in VC^ below values for air-saturated water with access to
air. The skin of these fish may assume up to 50% of the oxygen
uptake in air. Singh and Hughes (1971) found that 16% of the VO2
in air-saturated water was cutaneous. The amount of blood circulating
to the skin evidently increases upon emersion, as the skin of albino

53
individuals becomes pinker and cutaneous VC^ increases. Berg and
Steen (1965) found that cutaneous oxygen uptake of Anguilla vulgaris
is about 2.7 times greater in air than in water. The gills of
Ciarías also probably play an important role in aerial respiration,
as the widely spaced thickened lamellae would not collapse in air
and probably function similarly to those of species that employ
gill breathing in air, such as Symbranchus, Hypopomus and Periopthalmus.
The high aerial VC^ rates of Ciarías batrachus seem somewhat
inconsistent with some of the other aspects of the physiology of
this fish when it is exposed to air. Singh and Hughes (1971)
found that the respiratory quotient of C. batrachus in air was
lower (0.52) than other air-breathing forms they examined (Anabas
and Saccobranchus) even though Anabas is scaled. Howell (1970)
examined the buffering curves of blood of air-breathing fish
(including £. batrachus). These data, plus values for the carp
and bullfrog (from Rahn, 1967), are shown in Fig. 15; all values
are calculated for 25°C. Clarias and Neoceratodus, both primarily
water-breathers, have low HCO^ concentrations and are not capable
of buffering blood carbon dioxide much better than the carp. Howell
(1970) states that preliminary laboratory studies indicate that
Clarias goes into severe respiratory acidosis when forced to reside
in air for a few hours. Yet, Clarias is the only one of these air-
breathing fishes that has been reported to leave the water volun¬
tarily.
The skin of Clarias is very sensitive to desiccation and unless
it is kept moist, a few hours of air exposure produces necrosis of

Figure 15. Buffering capacity of blood of selected
vertebrates at 25°C (from Howell, 1970,
and Rahn, 1967).
A Electrophorus
B Rana
C Protopterus
D Lepidosiren
E Cyprinus
F Clarias
G
Neoceratodus

55
PH

56
the skin. Both the sensitivity of the skin and a propensity for
respiratory acidosis in air is probably why Ciarías leaves the water
and migrates mainly (if not exclusively) when it is raining. Ciarías
also follows thin sheets of runoff that flow over roads and down
into the ditches. These conditions maintain a film of water over
the animal's body surface, which prevents skin damage and presumably
would permit carbon dioxide elimination through the naked skin.
In water, Ciarías shows coupling of respiratory and circulatory
adaptations similar to other air-breathing forms such as Electrophorus,
Periophthalmus, and Symbranchus, as maximum cardiac output follows
an air breath. Inflation of the gill chamber in Ciarías corresponds
to an increase in heart rate from about 29 to 39 beats/minute.
Electrocardiograms of Ciarías show physiological features of a
terrestrially active fish such as Periophthalmus. After the
experimental tank was drained, heart rate fell to approximately
half the initial value until the fish moved and took a breath, then
tachycardia ensued with a 250% increase in heart rate. This is
very similar to the results obtained by Johansen (1966) for
Symbranchus. Gordon et al. (1970) found that the Chilean cling-
fish, Sicyases, a fish which is inactive upon emersion, showed an
immediate drop in heart rate upon removal from water. Heart rate
in this fish remained at low levels for the duration of their
emersion.
Clearly, Ciarías batrachus has many characteristics that have
contributed to its success in South Florida. It is able to survive
using aquatic respiration only in aerated water, until the PO2 drops

to very low levels. Air breathing is more common at night, which
tends to decrease susceptibility to predation by diurnally active
predators (herons). When oxygen tensions are low, fish survive by
breathing air and reducing the amount of activity. They can
survive drying (and probably cold in South Florida) by burrowing
in mud or making short excursions to deeper water. During the
rainy season they make extended excursions by water or land to
other waters, which contributes to the dispersal of these species
prior to breeding.

SUMMARY
1. Ciarlas batrachus is a facultative air breather.
2. The V00 of Ciarlas varies as a function of weight and access
to air. The metabolic rates of Ciarlas in air and water with
access to air are essentially the same, but the $C>2 of forcibly
submerged fish is lower.
3. The metabolism characteristic of forcibly submerged Ciarlas
is primarily aerobic, its reduced rate is probably the result
of reduced activity.
4. When the fish are in water with access to air, aquatic breath¬
ing accounts for 80-90% of the total oxygen uptake. Small
fish appear to increase aerial respiration at higher oxygen
tensions than do large fish.
5. Clarias are oxygen regulators at oxygen tensions above 40 mmHg.
6. The critical oxygen tension (Pc) of Clarias appears to
increase with increasing body weight, as it does in salamanders.
Because of the increased surface area for gas exchange provided
by the gills of Clarias, the values are about three times
l
lower than those of bimodally-breathing aquatic salamanders
(Siren).
7. The number of air breaths per unit time is a function of time
of day (doubles at night), and is inversely proportional to the
weight of fish. This may be due to the lack of a proportional
58

59
relationship between gill surface area and weight that is shown
in small Clarias (35-68 gms) , and also the proportionally
higher metabolic demands of small fish.
8. Oxygen uptake during air exposure is not reduced, as Clarias
is active upon emersion. Cutaneous oxygen uptake accounts for
up to 50% of the total VC^ in air-exposed fish. Cutaneous
vasodilation apparently occurs during emersion.
9. The high oxygen capacity of Clarias blood is probably an
adaptation to facilitate oxygen uptake because of the thickened
and somewhat reduced gill surface area that is necessary for
air breathing and terrestrial activity.
10. Electrocardiographic measurements of heart beat frequencies
demonstrate that Clarias is similar to other air breathers
that are well adapted to emersion.
11. It is suggested that the low HCO^ levels of the blood of
Clarias causing respiratory acidosis after brief periods of
air exposure and the sensitivity of the skin to desiccation
preclude terrestrial activity in Clarias except on rainy
nights when a cutaneous water film (essential for carbon
dioxide exchange) can be maintained.

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BIOGRAPHICAL SKETCH
Jill Ann Jordan was born in Columbia, South Carolina on February 20,
1944. She graduated from Niagara Falls High School in Niagara Falls,
New York and received a Bachelor of Science from Cornell University
in 1966. She received a Master of Science degree from Tulane University
in 1967, and enrolled in the University of Florida. Until the present
time, she has worked toward the Ph.D. in the Department of Zoology.
63

I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
B. K. McNab, Chairman
Professor and Chairman of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
F. G. Nordlie
Associate Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.
Pierce Brodkorb
Professor of Zoology
I certify that I have read this study and that in my opinion it
conforms to acceptable standards of scholarly presentation and is fully
adequate, in scope and quality, as a dissertation for the degree of
Doctor of Philosophy.

This dissertation was submitted to the Department of Zoology in the
College of Arts and Sciences and to the Graduate Council, and was
accepted as partial fulfillment of the requirements for the degree of
Doctor of Philosophy.
June, 1973
Dean, Graduate School

UNIVERSITY OF FLORIDA
3 1262 08556 7435



UNIVERSITY OF FLORIDA
3 1262 08556 7435