AMER. ZOOL., 13:799-818 (1973).
Endocrine Control of Hydromineral Balance in Teleosts
DONALD W. JOHNSON
Department of Biology, Idaho State University, Pocatello, Idaho 83201
and
Zoology Department and its Cancer Research Laboratory,
University of California, Berkeley, California 94720
SYNOPSIS. Hydromineral balance in teleosts is reviewed in an effort to define common
elements, as well as inter- and intra-species variation in its endocrine control.
Processes at the gill, gut, kidney, and urinary bladder are compared. The difficulty in
deriving functional generalities is discussed; the stimulation of both sodium influx and
efflux by cortisol, the ingestion of equal amounts of water by some fishes in either fresh
or sea water, and the equal glomerular filtration rates in both hypotonic and hypertonic environments for other fish confound such efforts at generalization. An attempt
is made to explain these inconsistencies through an examination of variation in hormonal balances and effector organ responses. Evidence for Na+/K+-ATPase involvement at the gill, gut, kidney, and urinary bladder is summarized. Patterns in cortisol
and prolactin availability as a function of synthesis, storage, and secretion are considered. A rather consistent antagonism of cortisol and prolactin in sodium movement and water permeability at several teleost effector organs is substantiated.
The massive and expanding literature
dealing with teleost hydromineral balance
and its endocrine control (recent reviews
include Maetz, 1970; Olivereau and Ball,
1970; Henderson et al., 1970; Lam, 1972;
Utida et al., 1972a) raises a question as to
the validity of simplistically restating the
historical dogmas of Smith (1932) and
Krogh (1939), regarding the maintenance of
hydromineral balance. Is renal production
of urine (glomerular nitration rate, GFR)
always reduced in seawater fishes as opposed to fishes in fresh water? Is the swallowing of water among teleosts a phenomenon confined to marine forms? While direct
correlation between the rate of water ingestion and salinity has been well documented
(Maetz and Skadhauge, 1968; Oide and
Utida, 1968), the absence of this correlation
Our research referred to herein was aided by NIH
grants CA-05388, CA-05045, and NSF grant GB23033 to H. A. Bern and an NIH fellowship to
D. W. J. We are indebted to the staff of the Bodega
Marine Laboratory of the University of California
for their generous cooperation. Kathleen Spiegel
and Emily Reid provided assistance with the figures.
Thanks are also due Drs. W. H. Sawyer, P. K. T.
Pang, and H. A. Bern for their critical reviews of
the manuscript and to Dr. T. Hirano for his essential contributions to our studies.
and the ingestion of significant quantities
of fresh water have been more recently substantiated (Maetz, 1970; Gaitskell and Chester Jones, 1971; Motais and Isaia, 1972;
Kirsch and Mayer-Gostan, 1972). A better
understanding of hormonal balances and
effector organ responses can help explain
water-conserving or -excluding mechanisms
that are operating in these "atypical" cases.
Teleosts maintain body fluids out of
phase with their aquatic media through correctional mechanisms involving the expenditure of energy and integration of gill, gut,
and renal function. With a great surface
area (integument, gills, and intestine) exposed to osmotic stress, survival requires
control systems sensitive to osmotic and
ionic fluctuations. Control is especially essential to euryhaline fishes which find themselves at different moments of their existence in both hypotonic and hypertonic
environments. Regulation of their hydromineral balance is not rigid, but within a
range that permits survival. In sea water
(SW), plasma sodium and osmolality generally exceed their levels in fresh water (FW)
by approximately 10% and 20%, respectively. These fishes—represented by eel
(Anguilla), flounder (Platichthys), and sal-
799
Epiphysis (pineal)
Pituitary hypothalamohypophysial system
Ultimobranchial
Urophysis
I
Urotensin HI
Corpuscles
of
Stannius
Mesonephric
kidney
Myeloid tissue
Head kidney
FIG. 1. Possible endocrine involvement in control of
osmoregulatory effector organs. Apparent diversity
o£ control may reflect imperfection or complexity of
hydromini'ral regulation. (Adapted from Bern, 1967.)
TELEOST HVDROMINERAL BALANCE
mon (Oncorhynchus)—are much studied
and have complex osmoregulatory control
patterns. Almost all endocrine glands in
fishes have been implicated in osmoregulatory conrol (Fig. 1).
Euryhaline teleosts maintain a relatively
constant serum sodium (140-165 mEq/1)
and osmolality (290-320 mOsm/1) whether
in a hypotonic (FW) or in a hypertonic
(SW) environment (see values from starry
flounder in Johnson et al., 1972). The role
of the epithelia of the gill, gut, gall bladder,
kidney, and urinary bladder, as well as the
skin, may be important in the maintenance
of this hydromineral balance. Changes in
osmotic permeability, active ion transport,
and rectification of flow are important
mechanisms in this regulation and respond
to variations in endocrine activity.
EVIDENCE OF ENDOCRINE INVOLVEMENT
The pituitary is undoubtedly the most
studied of the teleost endocrine organs.
Hypophysectomy precludes FW survival of
many species (Schreibman and Kallman,
1966, 1969). Burden (1956) described the
inability of the hypophysectomized mummichog (Fundulus heteroclitus) to maintain
plasma chloride at levels compatible with
survival in FW. He speculated that prolactin or some unknown adenohypophysial
factor was necessary for regulation in FW.
Evidence from hypophysectomized eel (Anguilla anguilla), mummichog, and sailfin
molly (Poecilia latipinna) indicates that
prolactin reduces sodium efflux in FW without affecting influx; in plains killifish (Fundulus kansae), influx is reduced with efflux
unaffected (Ball, 1969). Hypophysectomized
plains killifish lose sodium in FW but
nevertheless survive (Stanley and Fleming,
1967a), probably indicating that their movement of sodium and possibly their impermeability to water are not entirely prolactin-dependent. The influence of prolactin
on sodium regulation has been demonstrated, with a 40% reduction in efflux after
treatment of SW flounder (MacFarland, unpublished). Sage (personal communication)
has found a negative correlation between
pituitary prolactin and blood sodium con-
801
tent in striped mullet (Mugil cephalus) acclimating to FW which is absent in SW fish.
The increase in prolactin with decrease in
serum sodium in this euryhaline fish perhaps best demonstrates the involvement of
prolactin in osmoregulation. The ability of
prolactin to elevate plasma sodium and its
importance in the FW survival of numerous
other species have been well documented
(Pickford and Phillips, 1959; Ball and Ensor, 1965, 1967; Dharmamba et al., 1967;
Dharmamba, 1970). The histophysiological
evidence of prolactin involvement in osmoregulation and diadromous migrations has
been reviewed by Olivereau (1969). Seasonal (winter) inability of stickleback (Gasterosteus aculeatus), to survive in FW can
be reversed by prolactin treatment, another
ecological example of prolactin control
(Lam and Hoar, 1967; Lam and Leatherland, 1969). Seasonal variation in eel {Anguilla japonica) glomerular filtration rate
and urine flow rate (Oide, 1971) could be a
similar function of an annual cycle in prolactin secretion.
Prolactin treatment decreases Na+/K+ATPase activity at the gill, where sodium
efflux is also reduced, while increasing this
activity in the kidney, thus possibly contributing to renal sodium reabsorption at
this target organ (Epstein et al., 1969; Utida
et al., 1969; Pickford et al., 1970a). Lam's
(19696) results with in vitro stickleback gill
preparations and the muscle hydration studies in eel of Chan et al. (1968) support a
reduction of osmotic permeability in FW as
an effect of prolactin. Work recently completed by Ogawa and Yakasaki (cited in
Nicoll and Bern, 1971) confirmed Lam's
finding of reduced gill water permeability
following prolactin treatment. However, in
goldfish (Carassius auratus) and plains killifish, an increase in water permeability has
been suggested as a function of prolactin
(Stanley and Fleming, 1967b; Potts and
Fleming, 1970; Lahlou and Giordan, 1970).
In both fishes, hypophysectomy decreased
urine flow and increased urine sodium concentration; prolactin has an opposite effect. These findings suggest that prolactin
may decrease renal water permeability as it
does in the teleost bladder and gut (Johnson
802
DONALD W. JOHNSON
et al., 1970; Hirano et al., 1971; Utida and ship in activity has also been described from
Hirano, 1972; Johnson et al., 1972). This a histophysiological study of an estuarine
effect on the bladder may result from cell population of striped mullet. Stannius corproliferation inasmuch as thymidine incor- puscle tissue is most active in sea water
poration is increased by prolactin treat- (Johnson, 1972). Stannius corpuscle extract
ment. Bladder DNA synthesis parallels the elevates blood pressure and may act like the
decrease in water permeability and the in- renin-angiotensin system and/or be involved
crease in sodium transport (Hirano et al., in controlling corticoid secretion (Chester
1973a). The renotropic effect of prolactin Jones et al., 1965, 1966, 1969a; see also
is thought to involve increased GFR, re- Krishnamurthy and Bern, 1969). Reninduced water reabsorption, and reduced so- angiotensin has been identified from teleost
dium efflux (Lam, 1972). Lam suggested Stannius corpuscles, as well as from the
from the stimulation of urine flow and de- kidney (Sokabe et al., 1970; Capelli et al.,
creased urine sodium by prolactin that the 1970). A significant steroidogenic role for
excretion of the same or slightly higher the corpuscles seems to have been elimiamounts of sodium in prolactin-treated fish, nated by the study of Colombo et al. (1971).
considering the increased volume, indicated An interrelationship may exist between the
an increase in tubular reabsorption. Urine/ corpuscles and the ultimobranchial body.
plasma sodium ratios support this specula- Removal of the latter leads to reduced
tion. A corticotropic role for prolactin has plasma osmolality and atrophic Stannius
also been suggested, but prolactin treatment corpuscles. The removal of both glands rehas no effect on the interrenal tissue of sults in elevated plasma calcium. Whereas
mummichog, sailfin molly, or eel (Pickford removal of the corpuscles decreases urine
and Kosto, 1957; Chan et al., 1968; Ball and calcium, removal of the ultimobranchial
Ensor, 1969). In preliminary work on cor- body has the reverse effect (Chan, 1972). The
tisol levels in starry flounder (Platichthys possible role of the urophysis, the thyroid,
stellatus), ACTH produced a doubling of and renin-angiotensin in osmoregulation
serum cortisol; prolactin was without effect may be considered by other speakers at this
symposium.
(Johnson and Clarke, unpublished).
In general, present evidence seems to
The importance of interrenal tissue in the
regulation of hydromineral balance is also point to cortisol and prolactin as the domiwell established. Interrenalectomy results in nant hormonal factors in regulating hydroaltered plasma ion concentrations. In SW mineral balance with cortisol most critical
eel, sodium is elevated; in FW eel, it is in SW and prolactin in FW. Cortisol may
decreased (Mayer et al., 1967; Butler et al., act primarily at the ion pump level and
1969). This is indicative of the importance prolactin on osmotic permeability (Utida
of cortisol tofishesin both hypo- and hyper- et al., 1972a).
tonic media. In striped mullet, cortisol decreases serum sodium and potassium in SW, ENDOCRINE CONTROL AT THE EFFECTOR ORGAN
while the loss of these ions with transfer to
FW is reduced with cortisol treatment Integument
(Jackson and Sage, personal communication). The interrelationship of interrenal
In the teleost, with its scales and mucous
and Stannius corpuscle tissue appears to in- glands, the movement of water across the
volve compensatory activation of one by the integument has less osmoregulatory impact
removal of the other. Altered hydromineral than it does in some other aquatic vertebalance follows removal of either (Leloup- brates. Relative permeabilities for eel, river
Hatey, 1964; Chester Jones et al., 1966; lamprey, and frog in fresh water are 1:20:60
Fontaine, 1967; Mayer et al., 1967). "Stan- (Wikren, 1953); consequently, the skin as
niectomy" of FW eel decreases GFR and an osmoregulatory organ in teleosts has
plasma sodium (Fontaine, 1964; Chan et al., attracted little interest, and almost no firm
1967; Chan, 1972). This inverse relation- data have been collected, although sugges-
803
TELEOST HYDROMINERAL BALANCE
tions have been made regarding variation
in integumentary permeability with experimental treatment and fluctuating environmental salinity. The integument of eel
(Kirsch, 1972a) and rainbow trout (Shehadeh and Gordon, 1969) from SW is apparently almost totally impermeable to
water. Hypophysectomy reduces epidermal
mucous cells in teleosts, while prolactin reverses this effect (Schreibman and Kallman,
1965; Ogawa and Johansen, 1967; Ogawa,
1970). Transfer of stenohaline Anoptichthys
jordani to SW has an effect similar to hypophysectomy—reducing oral mucous cells;
transfer to FW or prolactin injection stimulates these cells (Mattheij and Sprangers,
1969).
Intestine:ingestion and absorption
Comparative drinking rates provide an
indication of permeability with "heavydrinking," an adaptation which compensates for greater permeability and reduced
renal reabsorption. Tilapia drink 27% body
wt/day in SW and 6% in FW (Potts et al.,
1967). Greater intraspecies variation with
habitat (SW:FW) has been reported for
rainbow trout (13:0), Japanese eel (A. japonica) (8:0) and European eel (A. anguilla)
(3.6:0.5) (Oide and Utida, 1968; Shehadeh
and Gordon, 1969; Gaitskell and Chester
Jones, 1971). The plains killifish, a euryhaline fish which, like the flounder, may be
exposed to a wide range of salinities (FW to
hypersaline) drink in an isotonic media
(33% SW) and respond to osmotic stress
with a 33% increase to 23% body wt/day,
increasing to 37% of their body weight/day
in hypersaline media (150% SW) (Potts and
Fleming, 1970). An initial increase in drinking rate with transfer to SW followed by a
decrease to FW levels has been reported for
both Japanese and European eel (Oide and
Utida, 1968; Kirsch and Mayer-Gostan,
1972). This can perhaps be explained as a
response accompanying the transitory increase in serum cortisol with transfer to SW
(Hirano, 1969). There are several relationships (patterns) between fish permeability
and drinking rate presumably regulated by
osmotic water loss, a function of surface
area and skin, gill, and renal permeabilities
which may be under endocrine control.
Hirano et al. (1972) have terminated the
drinking reflex in eels by vagotomy, whereas
drinking could not be stimulated by increased plasma osmolality, Mg 2+ , SO42+, or
Na+; only an increase in Cl~ or a decrease
in blood volume increased the drinking rate.
Decerebration, including hypophysectomy,
did not affect drinking in SW eels. Utida
et al. (19726) suggest a gill chloride receptor and a vagus-medulla-esophagus reflex.
Hypophysectomy of FW eel decreases their
water consumption, but is without effect in
SW eels (Gaitskell and Chester Jones, 1971).
This effect of hypophysectomy on drinking
rate may be a secondary response to the
absence of prolactin and a possible expanded blood volume resulting from increased osmotic permeability, rather than
reflecting a direct endocrine control of
drinking itself (Fig. 2).
As first shown by House and Green (1963)
and subsequently by others including Utida
et al. (1967), Oide and Utida (1967) and
SEfi WATER
FIG. 2. Hormonal control of water and sodium
movement at the integument and intestine (boxes
represent stomach, gall bladder and rectum). Open
arrows represent water movement; cross-hatched
arrows show sodium movement; inhibition is signified by a bar across the arrow; PRL (prolactin);
F (cortisol).
804
DONALD W. JOHNSON
Skadhauge and Maetz (1967), absorption as tonic. The rate of "solute-linked water flow"
well as (or instead of) ingestion may be reg- in the eel gut has been shown to be stimuulated by the osmotic gradient between the lated in a hypersaline (200% SW) environfish and its environment. The osmotic ment (Skadhauge, 1969). The adaptation of
gradient against which water absorption the SW eel gut for increased salt and water
takes place increases with adaptation to movement takes place after several days in
higher external salinity. Most of the water SW and is dependent on cortisol. Injection
swallowed, together with some salts, is ab- of FW eel with ACTH or cortisol after
sorbed from the intestine. This may be about 10 hours produces an increase in
illustrated by the sodium content of the active transport of sodium and permeability
rectal fluid (20 mEq/1) although both bile of the gut to water (Utida et al., 1972a). The
(277 mEq/1) and sea water (460 mEq/1) latent period may reflect the metabolic
which enter the gut are hypertonic to serum process of increasing Na+/K+-ATPase
(Hickman, 1968; Hunn, 1969a). Chloride activity. Intestinal levels of Na+/K+loss at the rectum is negligible in SW eels ATPase in hypophysectomized FW mum(Kirsch, 19726). Although in SW eel two- michog are unaffected by prolactin injecthirds of the chloride influx is at the gill, tions (Pickford etal., 1970a). Reduced levels
only one-third of the total chloride efflux in hypophysectomized SW fish are restored
is at the gill, negating the role of the SW to normal high levels by cortisol injection
gill in salt uptake with net movement at the (Pickford et al. 1970&). An increase in gut
gill being outward (Kirsch and Mayer- Na+/K+-ATPase activity has been reGostan, 1972). The gut is an osmotically ported in several SW-adapted and cortisolmore important site of sodium uptake even injected fishes (Oide, 1967; Jampol and Epthough less than 25% of the exchangeable stein, 1970; Pickford et al, 1970&). Cortisolsodium may be absorbed from the intestine injected FW eels respond with a color
of SW flounder (Motais and Maetz, 1965). change to the silver SW form, a reduction
In the flounder, 1 ^Eq/g/hour of sodium in serum electrolyte elevation with transmay be absorbed, and 1.7 /JEq/g/hour is fer to SW, and an increase in branchial and
absorbed in the eel; however, in stenohaline intestinal Na+/K+-ATPase (Epstein et
Serranus scriba this increases to 2.8 ^Eq/g/ al., 1971). These investigators concluded
hour, showing once more the magnitude of that this is "not likely to be an example of
interspecies variation in regulating hydro- the secondary adaptation of an enzyme to
mineral balance (Motais and Maetz, 1965; a primary increase in transport but rather
Maetz and Skadhauge, 1968; Maetz, 1969a). an instance of primary change in enzyme
Water is absorbed by following actively activity induced by a hormone." Smith and
transported sodium and chloride ions. The Ellory (1971), on the other hand, suggest
dependency of water movement on active that sodium transport and Na+/K+sodium transport was first shown by House ATPase activity may not be directly reand Green (1963) by using KCN to inhibit lated. A magnesium-dependent increase in
sodium movement from an in vitro gut alkaline phosphatase has also been correpreparation. Water movement increases lated with SW adaptation of the eel (Oide,
proportionately with stimulation of the 1970).
transport system and with increased osmotic
Water movement from the FW eel inpermeability; both of these conditions exist testine increases in autumn—the time of
in SW fishes (Utida and Hirano, 1972). The normal SW migration—while sodium upeffect of a hypertonic environment on ab- take at the gill decreases. The increased
sorption from the gut is also obvious from water influx is blocked by hypophysectomy
the rainbow trout data of Shehadeh and and can be subsequently restored by ACTH
Gordon (1969). They found that intestinal or cortisol. Prolactin treatment of SW eels
residues from trout in 33% SW were iso- has the opposite effect: water movement
tonic to plasma while residues from the gut decreases and sodium uptake at the gill inof trout in 50% or 100% SW were hypo- creases (Utida et al., 1969). In SW eel water
TELEOST HYDROMINERAL BALANCE
805
turnover rate is much greater than in FW.
Although cortisol is known to increase water
absorption at the gut, similar cortisol levels
in both SW and FW eel suggest the involvement of another factor (Gaitskell and Chester Jones, 1970). This other factor now appears to be the antagonistic presence of
prolactin in freshwater fish. Prolactin inhibition of water permeability and stimulation
of sodium absorption has been confirmed
for the eel intestine (Utida and Hirano,
1972). When SW is introduced into the gut
of a FW eel, sodium is absorbed but water
is not; both are absorbed following cortisol
injection (Utida et al., 1972&). While cortisol increases both active transport and
passive osmotic permeability, prolactin acts
antagonistically on the intestinal epithelium
reducing water permeability.
Evidence of SW-produced hypertrophy of
adrenocorticotropes and interrenal cells
have been reported in eel, although in
striped mullet and Atlantic salmon (Salmo
salar) similar cytological evidence indicates
hypertrophied interrenal tissue in FW (Olivereau, 1966; Hanke et al., 1967, 1969;
Johnson, 1972; Heyl and Carpenter, 1972).
Work recently completed in Sage's laboratory confirms increased interrenal activity
in FW mullet; Jackson (personal communication) has been unable to quantify cortisol
in SW fish while it is readily detected in
those from FW. Preliminary studies with
starry flounder also indicate a higher FW
level (7.8 ju.g/lOOmi) than those from SW
(5.0 yu,g/100ml) (Johnson and Mayer-Gostan, unpublished). Gaitskell and Chester
Jones (1970) found that water absorption
from FW eel gut is reduced following interrenalectomy and is restored by cortisol
injection. This supports the presence of a
cortisol effect in FW eel and the physiological importance of the antagonistic effect of prolactin on the gut of FW fish.
Hirano (1969) found that transfer of eel
from FW to SW produced only a transient
increase in plasma cortisol with similar
levels in eel adapted to either medium.
This transient increase was corroborated
by Forster, while the reciprocal transfer was
els with elevated levels only in estuarine
fish (Johnson and Colombo, unpublished).
Hirano and Utida (1971) conclude that prolonged augmentation of cortisol secretion
is unnecessary for the induction and maintenance of adaptive gill and gut changes in
sea water.
The importance of the gut in maintaining hydromineral balance apparently varies
greatly with species. Maetz and Skadhauge
(1968) found that sodium entering via the
gut was less than 1% of total intake in the
FW eel. In goldfish intestinal sodium absorption may approach 25% of that entering via the gills (J0rgenson and Rosenkilde,
1956). The contribution of the gut also
varies with feeding activity. Ingestion of
water by goldfish has been related to their
consumption of paniculate food material
(Allee and Frank, 1948). As to the importance of water absorption from the gut (or,
as later discussed, the urinary bladder), the
point has been made that in vitro preparations show only 20-25% of the movement
maintained in vivo (Utida and Hirano,
1972).
Comparative drinking rates show a relationship between "heavy-drinking" and increased permeability and reduced renal
absorption. Drinking habits vary greatly between fishes and with osmotic stress. Endocrine control of ingestion is doubtful, as
hypophysectomy is without effect on SW
fishes. Decreased blood volume or increased
chloride content increases drinking rate.
Absorption may, as with drinking, be stimulated by osmotic stress—be it FW or SW.
Here, also, a hypersaline environment produces an intensified response. Absorption,
unlike ingestion, is apparently under endocrine control. The adenohypophysial-interrenal axis is essential in SW, and prolactin
plays an important role in FW.
without effect (discussed in Henderson et
al., 1970). Field-collected samples of striped
mullet also have similar FW and SW lev-
times that of the skin (Parry, 1966). Gill
movement of tritiated water indicates that
virtually all water e.xcharige by Anguilla,
Gill
Most flux data not attributable to renal
exchange have been assumed to be at the
branchial level. The gills provide a susceptible osmotic membrane with a surface area
10 (Opsanus tau) to 60 (Scomber scombrus)
806
DONALD W. JOHNSON
Carassius, Platichthys, and Serranus occurs
at the gills (Motais et al., 1969). Permeability of the gill to water is less in SW than
FW. When gills from FW eels are incubated
in SW they lose more water than those from
SW fish, and metabolic inhibitors are without effect (Kamiya, 1967). Chloride cell activity increases in SW while mucous cells
decrease their secretion (Jozuka, 1966). The
action of prolactin on mucous cells and its
possible effect on membrane permeability
and osmoregulation have recently received
much attention (Lahlou and Sawyer, 1969;
Lahlou and Giordan, 1970; Stanley and
O'Connell, 1970; Dharmamba and Maetz,
1972). Euryhaline Platichthys flesus in SW
exchange 40% of their sodium each hour,
75% of which enters through the gills. In
stenohaline S. scriba, with greater permeability, 90% of sodium influx is via the gills
(Motais and Maetz, 1965). The importance
of this difference in permeability becomes
obvious with transfer from SW to FW, with
a decrease in sodium efflux of 90% in
Platichthys compared to 40% in Serranus;
Serranus rapidly expire in FW (Motais et
al., 1965). The ability to reduce permeability to sodium is essential to a euryhaline
habit. Gill efflux in FW is generally less
than 1% of the SW rate (Bentley, 1971).
"Solvent-drag" effect has been seen in the
gills of Serranus and Anguilla, but not in
Platichthys (Motais et al., 1969). This also
points to interspecific variability in hydromineral balance mechanisms.
In FW eel, interrenalectomy reduced
branchial sodium influx. Cortisol in physiological doses restored influx rate; however,
high doses increase efflux (Mayer et al.,
1967; Maetz, 1969a). A decrease in plasma
sodium can trigger increased gill influx in
the goldfish (Bourguet et al., 1964). Prolactin decreases sodium efflux in hypophysectomized FW sailfin molly, goldfish, eel, and
stickleback (Ball and Ensor, 1965, 1967;
Lam, 1968; Maetz et al., 1968; Lahlou and
Giordan, 1970), and in intact SW starry
flounder and Tilapia mossambica (Johnson
et al., 1972; Dharmamba et al., 1973). In
stickleback this has been suggested to involve stimulation of gill mucous cells
(Leatherland and Lam, 1969a). The coord-
ination of prolactin and cortisol activity in
at least euryhaline fishes in FW results in
the blocking of water uptake and the reduction of sodium efflux by prolactin and
the facilitation of sodium influx by cortisol
(Lam, 1969a; Hirano and Utida, 1971;
Johnson et al., 1972).
Our knowledge of the endocrine control
of osmoregulation by the teleost gill contains considerable contradictory information. Other chemical mediators that may be
involved include somatotropin, aldosterone,
vasotocin, isotocin, urotensin, acetylocholine, and adrenalin (Fig. 3). Aldosterone may
increase sodium influx at the gills of FW
eel and goldfish, or efflux as does cortisol in
seawater eel; it has also been credited with
diminishing efflux (Favre, 1960; Motais,
FRESH WATER
PRL
F(low),Aldo
AVT. IT
Adr.U
SEA WATER
Mhighl.Aldo
AVT
PRL.AIdo
Ach
PRL.AVT
Ach
chloride cell
k CT
differentiation
X"*'"
FIG. 3. Hormonal involvement in teleost hydromineral balance at the gill. PRL (prolactin), IT
(isotocin), rA (renin-angiotensin), Adr (adrenalin),
Ach (acetylcholine) , U (urotensin) , F (cortisol) ,
Aldo (aldosterone), AVT (arginine vasotocin),
STH (growth hormone), TSH (thyroid stimulating hormone), ACTH (adrenocorticotropic hormone) , GTH (gonadotropic hormone).
TELEOST HYDROMINERAL BALANCE
1967; Mayer and Maetz, 1967; Henderson
and Chester Jones, 1967). Although low
levels of aldosterone have been identified
in some FW fishes, a physiological role for
such low levels has not been demonstrated
(Chavin and Singley, 1972). Vasotocin and
oxytocin have been shown to facilitate
sodium efflux following transfer of flounder
from FW to SW (Motais and Maetz, 1967;
Maetz and Rankin, 1969). Vasotocin inhibits water turnover at the goldfish gill,
while both vasotocin and isotocin stimulate
sodium influx, possibly through increasing
the blood supply to chloride cells (Lahlou
and Giordan, 1970). Adrenalin stimulates
lamellar blood supply, increasing the exposure of these membranes to the surrounding media and osmotic stress (Steen and
Kruysse, 1964). Adrenalin has also been
credited with a direct stimulatory effect on
sodium uptake in the gills of rainbow trout,
with no relationship between flow rate or
pattern and gill sodium uptake (Richards
and Fromm, 1970). While adrenalin stimulates lamellar circulation, a form of "preventive osmoregulation" is attributed to the
"local hormone" acetylcholine which results in the bypass of lamellar capillary networks by the branchial circulation (Steen
and Kruysse, 1964).
Salinity tolerance of trout has been related to differentiation and growth. Smith
(1956) suggested that euryhaline migration
is initiated by endocrine control at metamorphosis and maturity (STH) or by overriding metabolic change. Maturation of
"chloride-cells" may be involved (Bentley,
1971). These mitochondria-rich cells at the
base of the gill lamellae undergo rapid renewal in SW Oncorhynchus with differentiation induced by increased serum sodium
(Conte and Lin, 1967). Na+/K+-ATPase
increases in the gills of some euryhaline
fishes in SW, including eel {A. japonica, A.
anguilla, and A. rostrata), mummichog,
rainbow trout, and the goby {Acanthogobius
flavimanus) (Utida et al., 1966; Epstein et
al., 1967; Kamiya and Utida, 1969; Motais,
1970; Jampol and Epstein, 1970). In euryhaline Crenimugil labosus and Dicentrarchus labrax, however, those acclimated to
FW have twice the gill Na+/K+-ATPase
807
level of those from SW. The marine origin
of these fishes is suggested as a possible explanation of this reverse pattern of enzyme
stimulation (Lasserre, 1971). The examination of gill values for 13 species of Japanese
stenohaline fishes disclosed lower levels of
activity in four FW species than in any of
the nine marine species (Utida and Hirano,
1972). These differences are positively correlated with chloride cell structure and
abundance. Gills from stenohaline SW species have four to five times the Na+/K+ATPase activity found in stenohaline FW
species (Kamiya and Utida, 1969; Jampol
and Epstein, 1970). Actinomycin D inhibits
both sodium efflux and Na+/K+-ATPase
(Maetz et al., 1969; Motais, 1970), The stimulation of branchial sodium efflux and
Na+/K+-ATPase with SW acclimation is
inhibited by hypophysectomy or adrenalectomy, which in turn is reversed with cortisol
injections (Epstein et al., 1967; Mayer et al.,
1967; Matez, 19696; Pickford et al., 1970b;
Kamiya, unpublished). A spring increase in
Na+/K+-ATPase activity in FW coho
salmon {Oncorhynchus kitsutch) prepares
them physiologically for migration; a decrease in July is associated with loss of this
"seawater drive" (Zaugg, 1970). Spring
smoltification of Japanese masu salmon (O.
masou) is accompanied by a doubling of
gill Na+/K+-ATPase activity, chloride
cell structural development, and increased
interrenal activity (Utida and Hirano, 1972).
In addition to the elevation of enzyme
levels in the gill of FW Japanese eel by
transfer to SW or cortisol treatment, the
levels are decreased with transfer from SW
to FW. Prolactin promotes this latter response, although it is without effect on SW
eels (Kamiya, 1972a,6). Prolactin also decreases enzyme activity in hypophysectomized FW mummichog (Pickford et al.,
1970a). The increase in Na+/K+-ATPase
and number of chloride cells, which occurs
in eel within one week of transfer from FW
to SW, gradually decreases until FW levels
are reached after one month's acclimation
(Shirai and Utida, 1970). Kamiya (1972a)
also found that the differences in SW eel
produced by hypophysectomy were absent
after one month. It appears, therefore, in at
808
DONALD W. JOHNSON
least this euryhaline teleost, A. japonica, the
mechanism is not solely regulated by the
ACTH-cortisol system. Alteration of cortisol
level apparently induces an increase; with
SW adaptation and decreased cortisol levels,
or with FW adaptation and increased prolactin levels, a decrease in gill activity is
apparent (Kamiya, 19726).
Differences in osmotic permeability may
result from variation in prolactin secretion
and release. In Tilapia, the rate of turnover
of body water is 115%/hr in FW and
84%/hr in SW (Potts et al., 1967). Comparative figures are 42% and 29% for eel and
31% and 20% for the flounder (Motais et
al., 1969). Nearly all water turnover is at the
gill, although adjustment through increased
urine flow (decreased absorption) in FW or
increased intestinal absorption in SW may
be critical to survival. Flounder, with the
greatest regulation of water permeability in
both FW and SW, apparently release all
prolactin secreted regardless of environmental media as contrasted to Tilapia
which may store prolactin in the pituitary
(Clarke, 1972). Prolactin variation in the
starry flounder is apparently more a function of stimulated secretory activity with
movement to FW than an elimination of
secretion and/or storage in SW, as seems the
case in Tilapia (Nagahama, personal communication). Demonstration of some, even
though minimal, adenohypophysial secretory activity in SW Tilapia and salmonids
(Dharmamba and Nishioka, 1968; Olivereau, 1969; McKeown, 1970) prompted Lam
(1972) to suggest some role for prolactin in
SW fishes.
Regulation of water and sodium turnover
at the extensive gill surface is essential to
teleost homeostasis, especially in euryhaline
fishes. Of the many hormones that have
been implicated in control of osmoregulation at the gill, once more, cortisol and prolactin seem the most critical. Both cortisol
and decreasing serum sodium stimulate
sodium influx, while prolactin decreases
sodium efflux and gill permeability to water.
Kidney and urinary bladder
As with the gill, the renal system plays a
dual role in euryhaline fishes, producing a
copious urine in fresh water, while in the
marine environment divalent ions absorbed
with swallowed sea water are flushed out
with minimal urine as most of the water of
the glomerular filtrate is conserved. In euryhaline fishes GFR is commonly decreased in
hypertonic and increased in hypotonic environments (Holmes and McBean, 1963;
Sharratt et al., 1964; Lahlou, 1966, 1967).
Renal reabsorption as well as GFR has a
role in hydromineral balance. In many
fishes it may be the primary adaptive mechanism. In FW fishes, less than 5% of the
glomerular filtrate may be reabsorbed suggesting that the renal tubule must be nearly
impermeable to water (Hickman, 1965). The
variability present in physiological adaptations to osmoregulation by euryhaline fishes
can be seen by comparing FW and SW
ratios for urine volume and GFR. These
are 6:5 in the eel (urine volume in FW is
6 times SW; GFR in FW is 5 times SW),
3:2 in flounder, and 133:16 in rainbow
trout, showing the range in control of both
GFR and renal reabsorption (Bentley,
1971). Eels reabsorb 24% and 40% of the
glomerular filtrate in FW and SW, respectively (Sharratt et al., 1964), flounder 57%
and 75% (Lahlou, 1967), and rainbow
trout 52% and 93% (Holmes and McBean,
1963). Variability in urine flow in goldfish
and flounder has been attributed to glomerular recruitment (Maetz, 1963; Lahlou,
1966). The reduction and stabilization of
flounder urine flow after 2 days in sea water
suggested to Lahlou (1967) that something
more than GFR was involved. Although the
greatest change in urine sodium and osmolality occurred within 16 hr, adjustment
was not complete until 48 to 72 hr after
salinity transfer. Plains killifish and eel display a gradual drop in urine flow within
hours (Fleming and Stanley, 1965; Chester
Jones et al., 19696). GFR of eel transferred
from FW to SW falls initially, although
within 10 days the SW GFR is equal to the
FW rate (Oide and Utida, 1968). Increased
tubular reabsorption in sea water is a possible compensating mechanism for this increased GFR. Rankin et al. (1972), using
perfused FW eel kidney, reported both
water and sodium reabsorption in excess of
TELEOST HYDROMINERAL BALANCE
90%. Sodium reabsorption is generally considered to take place in the distal segment
and collecting tubule (Hickman and
Trump, 1969). There is, however, no direct
physiological evidence for the roles of various segments of the renal tubule in water
and solute reabsorption and secretion. "Tubular" water reabsorption has been evaluated by differences between kidney and
bladder urine. In coho salmon migrating
from SW to FW and starry flounder transferred from SW to FW, a 15% reduction in
water reabsorption occurs (Miles, 1971;
Hirano et al., 1971). In hypertonic saltloaded goldfish, renal sodium loss is
decreased; reabsorption is stimulated (Bourquet et al., 1964). Hickman (1965) calculates 99.95% sodium reabsorption in pike
and Sharratt et al. (1964) 97.8% in the eel.
Greater renal sodium efflux in FW than in
SW is also characteristic of eel and flounder
(P. flesus) (Sharratt et al., 1964; Lahlou,
1967). This seems to be the case with P.
stellatus only when they are held in hypersaline (133%) SW, when renal filtrate reabsorption is apparently stimulated.
The renal role of neurohypophysial peptides characteristic of tetrapods is unclear in
fishes. They produce diuresis in goldfish and
eel, but are without effect in flounder
(Maetz et al., 1964; Maetz, 1968; Chester
Jones et al., 1969a; Johnson et al., 1972).
AVT may increase GFR as a result of
"glomerular recruitment" (Maetz et al.,
1964; Chester Jones et al., 1969a; Sawyer,
1972). Although AVT increases blood pressure in aglomerular Opsanus tau, diuresis
is not seen (Lahlou et al., 1969). AVT has
no stimulating effect on GFR in perfused
eel kidney while water reabsorption is increased. Urophysial extract, on the other
hand, decreases GFR as well as urine volume (Rankin et al., 1972). Urotensin increases osmotic permeability of in vitro toad
urinary bladder (Lacanilao, 1969) although
it is without effect on flounder bladder function (Johnson et al., 1972). Prolactin may
play an important role in "tubular" sodium
reabsorption. Hypophysectomized
FW
mummichog show increased renal Na+/
K+-ATPase after prolactin treatment
(Pickford et al., 1970a). Na+/K+-ATPase
809
level in the urinary bladder mucosa of FW
starry flounder is three times that found in
SW flounder, and prolactin treatment of
SW flounder results in a twofold increase
(Utida, Kamiya, Johnson, and Bern unpublished).
The elimination of copious amounts of
hypotonic urine from fish in fresh water, as
opposed to the small amounts of nearly isotonic urine voided by those in sea water, is
the only urine characteristic which appears
to hold for all teleosts. Urine flow is greatly
reduced by hypophysectomy in goldfish, and
increased urine salt loss is suspected in hyponatremic goldfish (Lahlou and Sawyer,
1969; Lahlou and Giordan, 1970). Reduced
urine flow in hypophysectomized plains
killifish is reversed by prolactin (Stanley
and Fleming, 1967&). Lahlou and Giordan
(1970) obtained similar results in prolactintreated goldfish while finding that cortisol
was without effect. These results are consistent with our finding using in vitro urinary bladders from flounder, although these
investigators, as well as Evans (1969) and
Potts and Fleming (1970), suggested that
prolactin increased membrane osmotic permeability as opposed to our finding of prolactin inhibition of water movement (Johnson et al., 1970, 1972; Hirano et al., 1971;
Utida et al., 1972a). After finding that prolactin and AVT are diuretic in goldfish and
that prolactin decreases urine sodium,
Lahlou and Giordan (1970) suggested that
"urine flow has its autonomous regulation
and does not merely reflect changes in external permeability to water." Cortisol plays
a role in urine production. GFR reduced by
interrenalectomy of FW eel is restored to
normal rate with cortisol (Chan et al.,
1969). Adrenalin, angiotensin, urophysial,
or Stannius corpuscle extracts may also increase urine flow in fresh water, possibly a
blood pressure effect (Chester Jones et al.,
1969a) (see Fig. 4).
Different primary target organs or merely
a difference in time of action of a hormone
on two target organs may exist in closely
related species. Brief osmotic adjustments
can be obtained by rapid regulation of urine
flow (GFR) and branchial influx. More
permanent adjustment may be delayed and
810
DONALD W. JOHNSON
PRL.AVT/AcSl,
F, UB. Ad'.U
Increase G F R
FRESH WATER
FIG. 4. Hormonal implication in regulation of teleost
hydromineral balance at the nephron and urinary
bladder. G. (glomerulus), N.S. (neck segment), P.T.
(proximal tubule), I.S. (intermediate segment), D.T.
(distal tubule), CD. (collecting duct), cSt (corpuscles of Stannius). G, I.S., and/or D.T. are absent
in some marine fishes.
require renal "tubular" adjustment. Possibly only "true" euryhaline fishes are capable of this adjustment in permeability. The
toadfish, a marine, sometimes euryhaline
fish, can enter fresh water but cannot reduce osmotic permeability nor increase
sodium reabsorption of the urinary bladder.
In FW it produces a nearly isotonic urine
with increased sodium loss (5 times SW loss).
A role for the urinary bladder in ion reabsorption is, however, supported by the near
absence of chloride in FW toadfish bladder
urine (Lahlou et al., 1969). Urine production can be regulated, which probably accounts for the increased sodium loss as well
as for their ability to frequent FW. Urinary
bladder function may play an important
role in periods of osmotic stress. The "true"
euryhaline fish capable of extended survival
in either FW or SW must regulate at both
gill and renal levels. Flounder may possess a
dual control pattern for both sodium influx
and efflux with instantaneous adjustment
followed by a delayed progressive change
(Maetz, 1970). Flounder transferred from
SW to FW rapidly reduce sodium efflux by
90%, followed after 30 min by further reduction. The efflux reduction in this euryhaline fish exceeds that of stenohaline Serranus by more than four times. The delayed
response consistently absent in stenohaline
fishes is suspected to be the result of endocrine control (Motais et al., 1966). Transfer
of starry flounder to a hypersaline environment produces an immediate elevation of
serum osmolality and sodium, which initiates the "adjustive" phase of Houston
(1959), probably regulated through sharp
decreases in GFR and gill influx. Adjustment appears complete after 7 days, which
is the lag period involved in elevation of
Na+/K+-ATPase. Increased serum magnesium during this time may provide the
stimulus for increased renal reabsorption
and increased gill efflux—the "regulatory"
phase. The initial phase may result from a
transitory cortisol elevation, and the lag
period may reflect decreasing blood titer
and/or tissue sensitivity to prolactin.
Lam (1972) concluded from the "granulerelease phenomenon" described by Leatherland (1970) and in vitro release of prolactin
from pituitary stimulation by dilute culture
media (Sage, 1968) that prolactin synthesis
and release are independently controlled,
with synthesis seasonally regulated and release dependent on ambient salinity. Prolactin secretion in starry flounder appears inhibited soon after transfer to a hypersaline
environment with pituitary content rising
sharply then falling to a low level after several days. The apparent decrease in prolactin secretion is followed by 48 hr with increased urinary bladder water permeability
which, in turn, is followed by decreasing
serum sodium levels. The reciprocal transfer—to fresh water—also produces a rapid
increase in pituitary prolactin activity which
is followed by exhaustion at 36 hr, another
high at 48 hr, and a nearly stabilized level at
72 hr. Urinary bladder water movement and
serum sodium reached apparent lows at 48
hr (Johnson, Hirano, Sage and Bern, unpublished). Potts and Evans (1967) noted a
greatly reduced sodium turnover in SW
mummichog within hours after brief exposure to FW. This reduction lasted for several hours suggesting hormonal control of
permeability in response to environmental
salinity. The prolactin time course data reported above support the role of prolactin
in the suggested regulatory pattern.
In marine Paralichthys lethostigma, the
TELEOST HYDROMINERAL BALANCE
GFR is high and urine flow is proportional,
as in most freshwater fishes. From this filtrate nearly all the sodium is reabsorbed,
leaving a predominantly divalent ion urine
(Hickman, 1968). Evidence has been presented for direct exchange of magnesium
and sodium and related to water movement
in the crab urinary bladder (Gross and
Capen, 1965). Natochin and Gusev (1970)
describe a similar relationship between magnesium and sodium in the renal function of
several teleosts, with magnesium chloride injections increasing sodium reabsorption and
magnesium excretion. Although changes in
urine osmolality and sodium concentration
depend largely upon changes in renal function, urinary bladder function may play an
important part in this function. Utilization
of the urinary bladder in hydromineral balance enables the kidney to flush out divalent ions and metabolic waste, a function
of importance in marine teleosts, while conserving water. This agrees with the view
that the primary function of urine production in SWfishesis not osmoregulation, but
divalent ion regulation and waste elimination (Krogh, 1939; Forster and Berglund,
1956).
The possibility of an osmoregulatory role
for the urinary bladder had been suggested
earlier as a result of catheterization studies
of urine which indicated a change in urine
composition in the bladder (Pitts, 1934;
Murdaugh et al., 1963; Lahlou, 1967; Lahlou et al., 1969). The histochemical and
ultrastructural similarities between known
water-impermeable ion-reabsorptive amphibian bladders and teleost terminal renal
structures led Hickman and Trump (1969)
to suggest such a role for the urinary bladder offishes.Through the use of an isolated
bladder preparation, this function in hydromineral balance has been elucidated and
substantiated, with the demonstration of
variation in water movement and sodium
transport with environmental salinity
(Johnson et al., 1970; Hirano et al., 1971,
19736). Prolactin is important in the inhibition of bladder osmotic permeability as
well as in the stimulation of sodium reabsorption (Hirano et al., 1971; Johnson et
al., 1972).
811
Recent studies suggest that cortisol may
also be a regulator of bladder function acting antagonistically to prolactin. Several observations suggested this possible role for
cortisol. Urine alteration following stress
led Hunn (19696) to conclude that electrolyte reabsorption was reduced by elevated
glucocorticoid levels. Urine flow (GFR?) is
maximal within 24 hr after stress of catheterization, while normal regulation is resumed after 48 hr (Hunn and Willford,
1970). Water movement (reabsorption) out
of FW starry flounder urinary bladder preparations is consistently less than 10%/hr;
bladders of approximately 95% of fish acclimated to a hypersaline media (133% SW)
exceed this level of water movement; the
area of possible overlap increased from 5%
to 25% in those acclimated to SW. Osmotic
stress—and elevated cortisol—of those fish
in 133% SW could account for the reduced
variability in these fish. Possibly the effect
of low level prolactin secretion on the urinary bladder in SW flounder may be reversed
only when cortisol is markedly increased.
Conversely, flounder collected under stressful conditions—high temperature and hypersaline water—and further stressed in the
laboratory fail to show a water movement
response to prolactin or FW transfer. Less
stressful handling leads to the earlier reported inhibition of bladder osmotic permeability with a single prolactin injection
or transfer to fresh water. The longjawed
mudsucker (Gillichthys mirabilis) responded
positively, with reduced osmotic permeability, to prolactin treatment when first tested.
Fish received a double injection of prolactin
(1 fxg/g body wt) at 24-hr intervals with
bladder water permeability assayed at 48
hr (Hirano et al., 19736). Subsequent attempts to duplicate this effect with five or
seven injections were unsuccessful; a return
to two injections reproduced the earlier prolactin bladder response. An antagonistic
role for cortisol is also suggested by the
failure of fish to show a positive correlation
between response and prolactin dose over a
wide range, but to respond maximally to
intermediate doses (Leatherland and Lam,
19696; Johnson et al., 1972). Preliminary
results of in vivo treatment of SW flounder
812
DONALD W. JOHNSON
F W - 10 days (3)
w /adrenalin chloride (4)
(0.25/jg/g. body wt.)
w/oldosterone (4)
(O.OI/jg/g. body wl.)
w/corlisol (3)
(l/ig/g. body wl.)
w/cortisol (4)
(IOjug/g,.body wt.)
133% SW - 10 days (12)
w/proloctin 113)
(Ijug/g body wt.)
•> corlisol (3)
(0.01 jug /g. body wt.)
* cortisol (4)
(O.I jug/g. body wt.)
+ cortisol (3)
U.Opg/q. body wt.)
t cortisol (3)
(10 jug/g. body wt)
-* cortisol (3)
(100 jug/g. body wt.)
w/prolactin (O.ljug/g) •
cortisol UOjug/g) (3)
w/prolactin ( I p g / g ) *
metopirone (2Ojug/g)-3 days (4)
w/metopirone - 3 days (3)
100
125
150
175
200
225
I
250
30
35
Serum Sodium (mEq /liter)
FW - 10 doys (3)
w/adrenalin chloride (4)
(0.25/jg/g body wl)
w/aldosterone (4)
(0.01 /jg/g. body wt.)
w/cortisol (3)
(l/jg/g. body wl.)
w/cortisol (4)
(lOjjg/g.body wt.)
133% SW - 10 days (12)
w/proloctin (13)
(Ijug/g body wl)
• cortisol (3)
(0.01 jug/g. body wt.)
•> cortisol (4)
(01 /jg/g. body wt.)
•t cortisol (3)
(lOjug/g body wl.)
•» cortisol (3)
110 jug/g body wt)
-*cortisol (3)
(100/jg/g body wt.)
w/prolactin (O.ljug/g) +
cartisol (!0jug/g)(3)
w/proloctin i\pq/q) *
metopiione (20/ig/g)-3 days (4)
w/ metopirone - 3 days (3)
10
15
Water Movement
20
25
TELEOST HYDRCmiN'ERAL BALANCE
with metopirone, or both prolactin and cortisol in a 1:100 ratio, appear to support a
role for cortisol as an antagonist of prolactin on the urinary bladder (Fig. 5).
Adrenalin and aldosterone together with
cortisol had previously been tested without
alteration of FW flounder urinary bladder
osmotic permeability (Johnson et al., 1972).
During the past year these hormones were
utilized again at what might be more realistic doses with two injections at 24-hr intervals and testing of bladder function 24 hr
after the second injection. Treatments were
again without effect (Fig. 5).
It appears, then, that the osmoregulatory
role of the starry flounder urinary bladder
may share the endocrine control system
demonstrated earlier for the gill and intestine with prolactin inhibiting water permeability and with cortisol reversing this
effect. While endocrine control of the urinary bladder may be indicative of renal
"tubular" reabsorption, endocrine control
of GFR and possible tubular secretion remains unclear.
REFERENCES
Allee, W. C, and P. Frank. 1948. Ingestion of colloidal material and water by goldfish. Physiol.
Zool. 21:381-390.
Ball, J. N. 1969. Prolactin and osmoregulation in
teleost fishes: a review. Gen. Comp. Endocrinol.
Suppl. 2:10-25.
Ball, J. N., and D. M. Ensor. 1965. Effect o£ prolactin on plasma sodium in the teleost, Poecilia latipinna. J. Endocrinol. 32:269-270.
Ball, J. N., and D. M. Ensor. 1967. Specific action of
prolactin on plasma sodium levels in hypophysectomized Poecilia latipinna (Teleostei). Gen. Comp.
Endocrinol. 8:432-440.
Ball, J. N., and D. M. Ensor. 1969. La specificite
zoologique des hormones hypophysaires et de leurs
FIG. BA and B. Responses of serum sodium and
flounder urinary bladder water movement response
in vitro to some in vivo hormonal treatments. Data
were treated by analysis of variance. Dunnett's procedure was used to compare treatment means with
the control mean and Tukey's w-procedure was used
to compare all means. Sample size and dosage are in
parentheses. A, In seawater fish, both prolactin and
metopirone produced a significant elevation of
serum sodium. An additive effect was seen when
they were injected together. The elevation produced
by prolactin was eliminated by the simultaneous
813
activites. Coll. Int. Centre Nat. Rech. Sci. 177:
215-224.
Bentley, P. J. 1971. Endocrines and osmoregulation.
Springer-Verlag, N. Y.
Bern, H. A. 1967. Hormones and endocrine glands
of fishes. Science. 158:455-462.
Bourguet, J., B. Lahlou, and J. Maetz. 1964. Modifications experimentales de l'equilibre hydromineral et osmoregulation chez Carassius auratus.
Gen. Comp. Endocrinol. 4:563-576.
Burden, C. E. 1956. The failure of hypophysectomized Fundulus heteroclitus to survive in fresh water. Biol. Bull. (W°° d s Hole) 110:8-28.
Butler, D. G., W. C. Clarke, E. M. Donaldson, and
R. W. Langford. 1969. Surgical adrenalectomy of
a teleost fish (Anguilla rostrata LeSeuer): effect
on plasma cortisol and tissue electrolyte and carbohydrate concentrations. Gen. Comp. Endocrinol.
12:503-514.
Capelli, J. P., L. C. Wesson, and G. E. Aponte. 1970.
A phylogenetic study of the renin-angiotensin
system. Amer. J. Physiol. 218:1171-1178.
Chan, D. K. O. 1972. Hormonal regulation of calcium balance in teleost fish. Gen. Comp. Endocrinol. Suppl. 3:411-420.
Chan, D. K. O., I. Chester Jones, I. W. Henderson,
and J. C. Rankin. 1967. Studies on the experimental alteration of water and electrolyte composition of the eel (Anguilla anguilla L.). J. Endocrinol. 37:297-317.
Chan, D. K. O., I. Chester Jones, and W. Mosley.
1968. Pituitary and adrenocortical factors in the
control of the water and electrolyte composition
of the freshwater European eel (Anguilla anguilla
L.). J. Endocrinol. 42:91-98.
Chan, D. K. O., J. C. Rankin, and I. Chester Jones.
1969. Influences of the adrenal cortex and the
corpuscles of Stannius on osmoregulation in the
European eel, Anguilla anguilla L., adapted to
fresh water. Gen. Comp. Endocrinol. Suppl. 2:
342-353.
Chavin, W., and J. A. Singley. 1972. Adrenocorticoids
of the goldfish (Carassius auratus L.). Comp.
Biochem. Physiol. 42:547-562.
Chester Jones, I., D. K. O. Chan, and J. C. Rankin.
1969a. Renal function in the European eel
(Anguilla anguilla L.): effects of the caudal neurosecretory system, corpuscles of Stannius, neurohy-
injection of cortisol. This antagonistic effect of
cortisol was seen with dosages 10 and 100X the
prolactin dosage. Treatment of fresh-water fish was
without effect. B, Water movement from urinary
bladders of seawater fish was significantly inhibited
by prolactin or metopirone. When cortisol was injected with prolactin in dosages 10 or 100X the
prolactin dosage, the significant inhibition of water
movement was eliminated. Urinary bladders of
fresh-water fish were unaffected by the treatments
tested.
814
DONALD W. JOHNSON
pophysial peptides and vasoactive substances. J.
Endocrinol. 43:21-31.
Chester Jones, I., D. K. O. Chan, and J. C. Rankin.
1969b. Renal function in the European eel
(Anguilla anguilla L.): changes in blood pressure
and renal function of the freshwater eel transferred to seawater. J. Endocrinol. 43:9-19.
Chester Jones, I., I. W. Henderson, D. K. O. Chan,
and J. C. Rankin. 1965. The role of the adrenal
cortex and the corpuscles of Stannius in the
electrolyte balance of the eel. Gen. Comp. Endocrinol. 5:669.
Chester Jones, I., I. W. Henderson, D. K. O. Chan,
J. J. Brown, A. F. Lever, J. I. S. Robertson, and
M. Tree. 1966. Pressor activity in extracts of
corpuscles of Stannius from the European eel
(Anguilla anguilla L.). J. Endocrinol. 34:393-408.
Clarke, W. C. 1972. Studies on the role and occurrence of prolactin in fishes. Ph.D. Dissertation,
University California, Berkeley.
Colombo, L., H. A. Bern, and J. Pieprzyk. 1971.
Steroid transformations by the corpuscles of Stannius and the body kidney of Salmo gairdnerii
(Teleostei). Gen. Comp. Endocrinol. 16:74-84.
Conte, F. P., and D. H. Y. Lin. 1967. Kinetics of
cellular morphogenesis in gill epithelium during
sea water adaptation of Oncorhynchus (Walhaum).
Comp. Biochem. Physiol. 24:945-957.
Dharmamba, M. 1970. Studies of the effects of
hypophysectomy and prolactin on plasma osmolarity and plasma sodium in Tilapia mossambica.
Gen. Comp. Endocrinol. 14:256-269.
Dharmamba, M., R. I. Handin, J. Nandi, and H. A.
Bern. 1967. Effect of prolactin on freshwater survival and on plasma osmotic pressure of hypophysectomized Tilapia mossambica. Gen. Comp.
Endocrinol. 9:295-302.
Dharmamba, M., and J. Maetz. 1972. Effects of
hypophysectomy and prolactin on the sodium
balance of Tilapia mossambica in fresh water.
Gen. Comp. Endocrinol. 19:175-183.
Dharmamba, M., N. Mayer-Gostan, J. Maetz, and
H. A. Bern. 1973. Effect of prolactin on sodium
movement in Tilapia mossambica adapted to sea
water. Gen. Comp. Endocrinol. (In press)
Dharmamba, M., and R. S. Nishioka. 1968. Response
of "prolactin-secreting" cells of Tilapia mossambica to environmental salinity. Gen. Comp. Endocrinol. 10:409-420.
Epstein, F. H., M. Cynamon, and W. McKay. 1971.
Endocrine control of Na-K-ATPase and seawater
adaptation in Anguilla rostrata. Gen. Comp. Endocrinol. 16:323-328.
Epstein, F. H., A. I. Katz, and G. E. Pickford. 1967.
Sodium- and potassium-activated adenosine triphosphates of gills: role in adaptation of teleosts
to salt water. Science 156:1245-1247.
Epstein, F. H., A. Manitius, E. Weinstein, A. J. Katz,
and G. E. Pickford. 1969. Sodium- and potassiumactivated adenosine triphosphatase in kidneys of
Fundulus heteroclitus adapted to fresh and salt
water. Yale J. Biol. Med. 41:388.
Evans, D. H. 1969. Studies on the permeability to
water of selected marine, freshwater, and euryhaline teleosts. J. Exp. Biol. 50:689-703.
Favre, L. C. 1960. Recherches sur l'adaptation de
Cyprins dores a des milieux de solinite diverse
et sur son determinisme endocrinien. Diplome
d'Etudes Superieures, Paris.
Fleming, W. R., and J. G. Stanley. 1965. Effects of
rapid changes in salinity on the renal function
of a euryhaline teleost. Amer. J. Physiol. 209:
1025-1030.
Fontaine, M. 1964. Corpuscules de Stannius et regulation ionique (Ca,K,Na) du milieu interieur de
l'Anguille (Anguilla anguilla L.). C. R. Hebd.
Seances Acad. Sci. 259:875-878.
Fontaine, M. 1967. Intervention des corpuscules de
Stannius dans l'equilibre phosphocalique du
milieu interieur d'un Poisson Teleosteen, l'Anguille. C. R. Hebd. Seances Acad. Sci. Ser. D
265:736-737.
Forster, R. P., and F. Berglund. 1956. Osmotic
diuresis and its effect on total electrolyte distribution in plasma and urine of the aglomerular
teleost, Lophius americanus. J. Gen. Physiol.
39:349-359.
Gaitskell, R. E., and I. Chester Jones. 1970. Effects
of adrenalectomy and cortisol injection on the
in vitro movement of water by the intestine of
the freshwater European eel {Anguilla anguilla
L.). Gen. Comp. Endocrinol. 15: 491-493.
Gaitskell, R. E., and I. Chester Jones. 1971. Drinking
and urine production in the European eel {Anguilla anguilla L.). Gen. Comp. Endocrinol. 16:
478-483.
Gross, W. H., and R. W. Capen. 1965. Some functions of the urinary bladder in a crab. Biol. Bull.
(Woods Hole) 131:272-291.
Hanke, W., K. Bergerhoff, and D. K. O. Chan. 1967.
Histological observations on pituitary ACTH-cells,
adrenal cortex, and the corpuscles of Stannius of
the European eel (Anguilla anguilla L.). Gen.
Comp. Endocrinol. 9:64-75.
Hanke, W., K. Bergerhoff, and D. K. O. Chan. 1969.
Histological and histochemical changes of organs
associated with adjustment to the environment.
Gen. Comp. Endocrinol. Suppl. 2: 331-341.
Henderson, I. W., D. K. O. Chan, T. Sandor, and
I. Chester Jones. 1970. The adrenal cortex and
osmoregulation in teleosts. Mem. Soc. Endocrinol.
18:31-55.
Henderson, I. W., and I. Chester Jones. 1967. Endocrine influence on the net extrarenal fluxes of
sodium and potassium in the European eel
(Anguilla anguilla L.). J. Endocrinol. 37:319-325.
Heyl, H. L., and S. J. Carpenter. 1972. Reversible
changes in adrenal cortical cell morphology and
plasma hydroxycorticosteroids during freshwater
portion of the spawning journey of Atlantic
salmon (Salmo salar). J. Fish. Res. Board Can.
29:311-314.
Hickman, C. P., Jr. 1965. Studies on renal function
in freshwater teleost fish. Trans. Roy. Soc. Can.
3:213-236.
Hickman, C. P., Jr. 1968. Ingestion, intestinal ab-
TELEOST HYDROMINERAL BALANCE
sorption and elimination of sea water and salt in
the southern flounder, Paralichthys lethostigma.
Can. J. Zool. 46:457-466.
Hickman, C. P., Jr. and B. F. Trump. 1969. The
kidney, p. 91-239. In W. S. Hoar and D. J. Randall
[ed.], Fish physiology. Vol. I. Academic Press, N.Y.
Hirano, T. 1969. Effects of hypophysectomy and
salinity change on plasma cortisol concentration
in the Japanese eel, Anguilla japonica. Endocrinal.
Jap. 16:557-560.
Hirano, T., S. Hayashi, and S. Utida. 1973a. Stimulatory effect of prolactin on incorporation of (3H)thymidine into the urinary bladder of the flounder
(Kareius bicoloralus). J. Endocrinol. (In press)
Hirano, T., D. W. Johnson, and H. A. Bern. 1971.
Water movement in isolated flounder urinary
bladder and its hormonal control by prolactin.
Nature (London) 230:469-471.
Hirano, T., D. W. Johnson, H. A. Bern, and S.
Utida. 19736. Studies on water and ion movements
in the isolated urinary bladder of selected freshwater, marine, and euryhaline teleosts. Comp.
Biochem. Physiol. (In press)
Hirano, T., M. Satou, and S. Utida. 1972. Central
nervous system control of osmoregulation in the
eel (Anguilla japonica). Comp. Biochem. Physiol.
43A:537-544.
Hirano, T., and S. Utida. 1971. Plasma cortisol concentration and the rate of intestinal water absorption in the eel Anguilla japonica. Endocrinol.
Jap. 18:47-52.
Holmes, W. N., and R. W. McBean. 1963. Studies on
the glomerular filtration rate of rainbow trout
(Salmo gairdneri). J. Exp. Biol. 40:335-341.
House, C. R., and K. Green. 1963. Sodium and water
transport across isolated intestine of a marine
teleost. Nature (London) 199:1293-1294.
Houston, A. H. 1959. Osmoregulatory adaptation of
steelhead trout (Salmo gairdneri Richardson) to
sea water. Can. J. Zool. 37:729-748.
Hunn, J. B. 1969a. Inorganic composition of gallbladder bile from fasted rainbow trout. Progr.
Fish Cult. 31:221-222.
Hunn, J. B. 19696. Chemical composition of rainbow trout urine following acute hypoxic stress.
Trans. Amer. Fish. Soc. 98:20-22.
Hunn, J. B., and W. A. Willford. 1970. The effect
of anesthetization and urinary bladder catheterization on renal function of rainbow trout. Comp.
Biochem. Physiol. 33:805-812.
Jampol, L. M., and F. H. Epstein. 1970. Sodiumpotassium-activated adenosine-triphosphatase and
osmotic regulation by fishes. Amer. J. Physiol.
218:607-611.
Johnson, D. W. 1972. Variations in the interrenal
and corpuscles of Stannius of Mugil cephalus
from the Colorado River and its estuary. Gen.
Comp. Endocrinol. 19:7-25.
Johnson, D. W., H. A. Bern, and T. Hirano. 1972.
Water and sodium movements and their hormonal
control in the urinary bladder of the starry
flounder (Platichthys stellalus). Gen. Comp. Endocrinol. 19:115-128.
815
Johnson, D. W., T. Hirano, and H. A. Bern. 1970.
Water and sodium movements in flounder (Platichthys stellatus) urinary bladder and their hormonal control. Amer. Zool. 10:497.
J0rgensen, C. B., and P. Rosenkilde. 1956. On regulation and content of chloride in goldfish. Biol.
Bull. (Woods Hole) 110:300-305.
Jozuka, K. 1966. Chloride-excreting and mucus secreting cells in the gills of the Japanese common
eel. Annot. Zool. Jap. 39:202-210.
Kamiya, M. 1967. Changes in ion and water transport in isolated gills of the cultured eel during
the course of salt adaptation. Annot. Zool. Japon.
40:123-129.
Kamiya, M. 1972a. Sodium-potassium-activated adenosinetriphosphatase in isolated chloride cells from
eel gills. Comp. Biochem. Physiol. (In press)
Kamiya, M. 19726. Hormonal regulation of Na-KATPase activity in eel gills with special reference
to seawater adaptation. Endocrinol. Jap. (In press)
Kamiya, M., and S. Utida. 1969. Sodium-potassiumactivated adenosinetriphosphatase activity in gills
of freshwater, marine, and euryhaline teleosts.
Comp. Biochem. Physiol. 31:671-674.
Kirsch, R., 1972a. The kinetics of peripheral exchanges of water and electrolytes in the silver eel
in fresh water and sea water. J. Exp. Biol. (In
press)
Kirsch, R. 19726. Plasma chloride and sodium, and
chloride space in the European eel, Anguilla
anguilla L. J. Exp. Biol. (In press)
Kirsch, R., and N. Mayer-Gostan. 1972. Kinetics of
water and chloride exchanges during adaptation
of the European eel to seawater. J. Exp. Biol.
(In press)
Krishnamurthy, V. G., and H. A. Bern. 1969. Correlative histologic study of the corpuscles of
Stannius and the juxtaglomerular cells of teleost
fishes. Gen. Comp. Endocrinol. 13:313-335.
Krogh, A. 1939. Osmotic regulation in aquatic
animals. Cambridge Univ. Press.
Lacanilao, F. 1969. Teleostean urophysis: stimulation of water movement across the bladder of the
toad, Bufo marinus. Science 163:1326-1327.
Lahlou, B. 1966. Mise en evidence d'un "recruitement glomerulaire" dans le rein des T£leost6ens
d'apres la mesure du Tm glucose. C. R. Hebd.
Seances Acad. Sci. 262:1356-1358.
Lahlou, B. 1967. Excretion r£nale chez un poisson
euryhalin, le flet (Platichthys fiesus L.): caracteristiques de l'urine normale en eau douce et en eau
de mer et effets des changements de milieu. Comp.
Biochem. Physiol. 20:925-938.
Lahlou, B., I. W. Henderson, and W. H. Sawyer.
1969. Renal adaptations by Opsanus tau, a euryhaline aglomerular teleost, to dilute media. Amer.
J. Physiol. 216:1266-1272.
Lahlou, B., and A. Giordan. 1970. Le contrfile hormonal des ^changes et de la balance de l'eau chez
le Tele'oste'en d'eau douce Carassius auratus, intact
et hypophysectomise'. Gen. Comp. Endocrinol.
14:491-509.
Lahlou, B., and W. H. Sawyer. 1969. Electrolyte
816
DONALD W. JOHNSON
balance in hypophysectomized goldfish, Carassius
auratus L. Gen. Comp. Endocrinol. 12:370-377.
Lam, T. J. 1968. Effect of prolactin on plasma electrolytes of the early-winter marine threespine
stickleback, Gasterosteus aculeatus form trachurus,
following transfer from sea to fresh water. Can. J.
Zool. 46:1095-1097.
Lam, T. J. 1969a. A new technique for the collection
of urine of small fishes and for the study of
materials via the head region. Can. J. Zool. 47:
225-228.
Lam, T. J. 1969ft. The effect of prolactin on osmotic
influx of water in isolated gills of the marine
threespine stickleback Gasterosteus aculeatus L.,
form trachurus. Comp. Biochem. Physiol. 31:909913.
Lam, T. J. 1972. Prolactin and hydromineral regulation in fishes. Gen. Comp. Endocrin. Suppl. 3:
328-338.
Lam, T. J., and W. S. Hoar. 1967. Seasonal effects of
prolactin on freshwater osmoregulation of the
marine form (trachurus) of the stickleback Gasterosteus aculeatus. Can. J. Zool. 45:509-516.
Lam, T. J., and J. F. Leatherland. 1969. Effect of
prolactin on freshwater survival of the marine
form {trachurus) of the threespine stickleback,
Gasterosteus aculeatus, in the early winter. Gen.
Comp. Endocrinol. 12:385-394.
Lasserre, P. 1971. Increase of the (Na+ + K+)dependent ATPase activity in gills and kidneys
of two euryhaline marine teleosts Crenimugil
labosus (Risso, 1826) and Dicentrarchus labrax
(Linnaeus, 1758) during adaptation to fresh water.
LifeSci. 10:113-119.
Leatherland, J. F. 1970. Seasonal variation in the
structure and ultrastructure of the pituitary of
the marine form (trachurus) I. Rostral pars distalis. Z. Zellforsch. Mikroskop. Anat. 104:301-317.
Leatherland, J. F., and T. J. Lam. 1969a. Effect of
prolactin on the density of mucous cells on the
gill filaments of the marine form (trachurus) of
the threespine stickleback, Gasterosteus aculeatus
L. Can. J. Zool. 47:787-792.
Leatherland, J. F., and T. J. Lam. 1969&. Prolactin
and survival in deionized water of the marine
form (trachurus) of the threespine stickleback,
Gasterosteus aculeatus L. Can. J. Zool. 47:989-996.
Leloup-Hatey, J. 1964. Influence d'un apport sodique
et de l'aldosterone sur le dese'quilibre mineral
cons^cutif a l'ablation des corpuscles de Stannius
chez l'anguille Anguilla anguilla L. C. R. Seances
Soc. Biol. 158:991-994.
Maetz, J. 1963. Physiological aspects of neurohypophysial function in fishes with some reference to
the amphibia. Symp. Zool. Soc. London 9:107-140.
Maetz, J. 1968. Salt and water metabolism, p. 47-162.
In E. J. W. Barrington and C. B. J0rgensen [ed.],
Perspectives in endocrinology: hormones in the
lives of lower vertebrates. Academic Press, New
York.
Maetz, J. 1969a. Observations on the role of the
pituitary-interrenal axis in the regulation of the
eel and other teleosts. Gen. Comp. Endocrinol.
Suppl. 2:299-316.
Maetz, J. 1969&. Seawater teleosts: evidence for a
sodium-potassium exchange in the branchial
sodium-excreting puinp. Science 166:613-615.
Maetz, J. 1970. Mechanisms of salt and water transfer across membranes in teleosts in relation to the
aquatic environment. Mem. Soc. Endocrinol. 18:
3-29.
Maetz, J., J. Bourguet, B. Lahlou, and J. Hourdry.
1964. Peptides neurohypophysaires et osmoregulation chez Carrassius auratus. Gen. Comp. Endocrinol. 4:508-522.
Maetz, J., R. Motais, and N. Mayer. 1968. Isotopic
kinetic studies on the endocrine control of teleostean ionoregulation, p. 225-232. Proc. 3rd Int.
Congr. Endocrinol. Excerpta Med. Int. Congr. Ser.
No. 184.
Maetz, J., J. Nibelle, M. Bornancin, et R. Motais.
1969. Action sur l'osmordgulation de l'Anguille
de divers antibiotiques inhibiteurs de la synthese
des proteines ou du r£nouvellement. Comp. Biochem. Physiol. 30:1125-1151.
Maetz, J., and J. C. Rankin. 1969. Quelques aspects
du role biologiques des hormones neurohypophysaires chez les Poissons. Colloq. Int. Centre
Nat. Rech. Sci. 177:45-54.
Maetz, J., and E. Skadhauge. 1968. Drinking rates
and gill ionic turnover in relation to external
salinities in the eel. Nature (London) 217:371-373.
Mayer, N., et J. Maetz. 1967. Axe hypophysointerreiialien et osmordgulation chez l'Anguille en
eau de mer. Etude de l'animal intact avec notes
sur les perturbations de l'dquilibre mineral produites par l'effet de "choc". C. R. Hebd. Seances
Acad. Sci. 264:1632-1635.
Mayer, N., J. Maetz, D. K. O. Chan, M. Forster,
and I. Chester Jones. 1967. Cortisol, a sodium
excretive factor in the eel (Anguilla anguilla L.)
adapted to sea water. Nature (London) 214:11181120.
Mattheij, J. A. M., and J. A. P. Sprangers. 1969. The
site of prolactin secretion in the adenohypophysis
of the stenohaline teleost, Anoptichthys jordani,
and the effects of this hormone on mucous cells.
Z. Zellforsch. 99: 411-419.
Miles, H. M. 1971. Renal function in migrating
adult coho salmon. Comp. biochem. Physiol. 38:
787-826.
McKeown, B. A. 1970. Immunilogical identification
and quantification of pituitary hormones in
sockeye salmon (Oncorhynchus nerka, Walbaum).
Ph.D. Dissertation, Simon Fraser University, British Columbia, Canada.
Motais, R. 1967. Les me'canismes d'^changes ioniques
branchiaux chez les T61£ost£ens. Leur r61e dans
l'osmor£gulation. Ann. Inst. Oceanogr. 5:1-83.
Motais, R. 1970. Effect of actinomycin D on the
branchial Na-K dependent ATPase activity in
relation to sodium balance of the eel. Comp.
Biochem. Physiol. 34:497-501.
Motais, R., F. Garcia Romeu, and J. Maetz. 1965.
M<5canisme de l'euryhalinit£. Etude comparee du
Fkt (eurjhalin) et du Senan (sttnohalin) au cours
TELEOST HYDROMINERAL BALANCE
du transfert en eau douce. C. R. Hebd. Seances
Acad. Sd. 261:801-804.
Motais, R., F. Garcia Romeu, and J. Maetz. 1966.
Exchange diffusion effect and euryhalinity in
teleosts. J. Gen. Physiol. 50:391-422.
Motais, R., and J. Isaia. 1972. Temperature dependence of permeability to water and to sodium of
the gill epithelium of the eel (Anguilla anguilla).
J. Exp. Biol. 56:587-600.
Motais, R., J. Isaia, J. C. Rankin, and J. Maetz. 1969.
Adaptive changes of the water permeability of the
teleostean gill epithelium in relation to external
salinity. J. Exp. Biol. 51:529-546.
Motais, R., and J. Maetz. 1965. Comparaison des
echanges de sodium chez un Teleostien euryhalin
(le Flet) et un Teleost£en stenohalin (le Serran)
en eau de mer. Importance relative du tube
digestif et de la branchie dans ces echanges. C. R.
Hebd. Seances Acad. Sci. 261:532-535.
Motais, R., and J. Maetz. 1967. Arginine vasotocine
et evolution de la permeability branchiale au
sodium au cours du passage d'eau douce en eau
de mer chez le Flet. J. Physiol. (Paris) 59:271.
Murdaugh, H. V. Jr., P. Soteres, W. Pyron, and E.
Weiss. 1963. Movement of inulin and bicarbonate
ion across the bladder of aglomerular teleost,
Lophius americanus. J. Clin. Invest. 42:959.
Natochin, Y. V., and G. P. Gusev. 1970. The coupling
of magnesium secretion and sodium reabsorption
in the kidney of teleost. Comp. Biochem. Physiol.
37:107-111.
Nicoll, C. S., and H. A. Bern. 1971. On actions of
prolactin among the vertebrates: Is there a common denominator?, p. 299-324. In G. E. W.
Wolstenholme and J. Knight [ed.], Lactogenic
hormones CIBA Foundation.
Ogawa, M. 1970. Effects of prolactin on the epidermal mucous cells of the goldfish, Carassius
auratus L. Can. J. Zool. 48:501-503.
Ogawa, M., and P. H. Johansen. 1967. A note on the
effects of hypophysectomy on the mucous cells of
the goldfish, Carassius auratus L. Can. J. Zool.
45:885-886.
Oide, H. 1967. Effects of inhibitors on transport of
water and ion in isolated intestine and Na+ - K*
ATPase in intestinal mucosa of the eel. Annot.
Zool. Jap. 40:130-135.
Oide, H. 1970. Purification and some properties of
alkaline phosphatase from intestinal mucosa of the
eel adapted to fresh water or sea water. Comp.
Biochem. Physiol. 36:241-252.
Oide, H. 1971. Annual variation of renal function in
freshwater Japanese eel (Anguilla japonica). Zool.
Mag. 80:58-60.
Oide, M., and S. Utida. 1967. Changes in water and
ion transport in isolated intestines of the eel during salt adaptation and migration. Mar. Biol.
1:102-106.
Oide, H., and S. Utida. 1968. Changes in intestinal
absorption and renal excretion of water during
adaptation to sea-water in the Japanese eel. Mar.
Biol. 1:172-177.
Olivereau, M. 1966. Influence d'un sejour en eau
817
demineralisee sur le systeme hypophyso-surrenalien
de l'Anguille. Ann. Endocrinol. 27:665-678.
Olivereau, M. 1969. Functional cytology of prolactin
secreting cells. Gen. Comp. Endocrinol. Suppl.
2:32-41.
Olivereau, M., and J. N. Ball. 1970. Pituitary influences on osmoreguladon in teleosts. Mem. Soc.
Endocrinol. 18:57-85.
Parry, G. 1966. Osmotic adaptation in fishes. Biol.
Rev. 41:392-444.
Pickford, G. E., R. W. Griffith, J. Torretti, E.
Hendler, and F. H. Epstein. 1970a. Branchial
reduction and renal stimulation of (Na*, K+)ATPase by prolactin in hypophysectomized killifish in fresh water. Nature (London) 228:378-379.
Pickford, G. E., and B. Kosto. 1957. Hormonal induction of melanogenesis in hypophysectomized
killifish (Fundulus heteroclitus). Endocrinology
61:177-196.
Pickford, G. E., P. K. T. Pang, E. Weinstein, J.
Torretti, E. Hendler, and F. H. Epstein, 19706.
The response of the hypophysectomized cyprinodont, Fundulus heteroclitus, to replacement
therapy with cortisol: Effects on blood serum
and sodium-potassium activated adenosine triphosphate in the gills, kidney, and intestinal
mucosa. Gen. Comp. Endocrinol. 14: 524-534.
Pickford, G. E., and J. G. Phillips. 1959. Prolactin,
a factor in promoting survival of hypophysectomized killifish in freshwater. Science 130:454-455.
Pitts, R. F. 1934. Urinary composition in marine
fish. J. Cell. Comp. Physiol. 4:389-395.
Potts, W. T. W., and D. H. Evans. 1967. Sodium and
chloride balance in the killifish Fundulus heteroclitus. Biol. Bull. (Woods Hole) 133:411-425.
Potts, W. T. W., M. A. Foster, P. P. Rudy, and G. P.
Howells. 1967. Sodium and water balance in the
cichlid teleost, Tilapia mossambica. J. Exp. Biol.
47:461-470.
Potts, W. T. W., and W. R. Fleming. 1970. The
effects of prolactin and divalent ions on the permeability to water of Fundulus hansae. J. Exp.
Biol. 53:317-327.
Rankin, J. C, N. G. Moss, and M. M. Babiker. 1972.
Study of urine production by a perfused kidney
preparation of the eel (Anguilla anguilla L.) with
special reference to hormone actions. Gen. Comp.
Endocrinol. 18:618.
Richards, B. D., and P. O. Fromm. 1970. Sodium
uptake by isolated perfused gills of rainbow trout
(Salmo gairdneri). Comp. Biochem. Physiol. 33:
131-310.
Sage, M. 1968. Responses to osmotic stimuli of
Xiphophorus prolactin cells in organ culture.
Gen. Comp. Endocrinol. 10:70-74.
Sawyer, W. H. 1972. Neurohypophyseal hormones
and water and sodium excretion in the African
lungfish. Gen. Comp. Endocrinol. Suppl. 3:345-349.
Schreibman, M. P., and K. D. Kallman. 1965. The
effect of hypophysectomy on freshwater survival
and scale mucous cells in two species of freshwater
fishes. Amer. Zool. 5:728. (Abstr.)
Schreibman, M. P., and K. D. Kallman. 1966. Endo-
818
DONALD W. JOHNSON
crine control of freshwater tolerance in teleosts.
Gen. Comp. Endocrinol. 6:144-155.
Schreibman, M. P., and K. D. Kallman. 1969. The
effect of hypophysectomy on freshwater survival
in teleosts of the order Atheriniformes. Gen.
Comp. Endocrinol. 13:27-38.
Sharratt, B. M., I. Chester Jones, and D. Bellamy.
1964. Water and electrolyte composition of the
body and renal function of the eel (Anguilla
anguilla L.). Comp. Biochem. Physiol. 11:9-18.
Shehadeh, Z. H., and M. S. Gordon. 1969. The role
of the intestine in salinity adaptation of the
rainbow trout, Salmo gairdneri. Comp. Biochem.
Physiol. 30:397-418.
Shirai, N., and S. Utida. 1970. Development and
degeneration of the chloride cell during seawater
and freshwater adaptation of the Japanese eel,
Anguilla japonica. Z. Zellforsch. 103:247-264.
Skadhauge, E. 1969. The mechanism of salt and
water absorption in the intestine of the eel (Anguilla anguilla) adapted to waters of various
salinities. J. Physiol. (London) 204:135-158.
Skadhauge, E., and J. Maetz. 1967. Etude in vivo de
l'absorption intestinale d'eau et d'electrolytes chez
Anguilla anguilla adapts a des milieux de salinities diverses. C. R. Hebd. Seances Acad. Sci. 265:
347-350.
Smith, D. C. W. 1956. The role of the endocrine
organs in the salinity tolerance of trout. Men. Soc.
Endocrin. 5:83-101.
Smith, H. W. 1932. Water regulation and its evolution in fishes. Quart. Rev. Biol. 7: 1-26.
Smith, M. W., and J. C. Ellory. 1971. Temperatureinduced changes in sodium transport and Na*/
K+-adenosine triphosphatase activity in the intestine of goldfish (Carassius auratus L.). Comp.
Biochem. Physiol. 39A:209-218.
Sokabe, H., H. Nishimura, M. Ogawa, and M. Oguri.
1970. Determination of renin in the corpuscles of
Stannius of the teleost. Gen. Comp. Endocrinol.
14:510-516.
Stanley, J. G., and W. R. Fleming. 1967a. The effect
of hypophysectomy on the electrolyte content of
Fundulus kansae held in fresh and sea-water.
Comp. Biochem. Physiol. 20:489-497.
Stanley, J. G., and W. R. Fleming. 19676. Effect of
prolactin and ACTH on the serum and urine
sodium levels of Fundulus kansae. Comp. Biochem. Physiol. 20:199-208.
Stanley, J. G., and J. K. O'Connell. 1970. Effects of
hypophysectomy on plasma electrolytes and epidermal mucous cells in the mudminnow, Umbra
limi. Amer. Zool. 10:298. (Abstr.)
Steen, J. B., and A. Kruysse. 1964. The respiratory
function of teleostean gills. Comp. Biochem.
Physiol. 12: 127-142.
Utida, S., and T. Hirano. 1972. Effects of changes in
environmental salinity on salt and water movement in the intestine and gills of the eel, Anguilla
japonica. In W. Chavin and N. Egami [ed.], Responses of fishes to environmental change. (In
press)
Utida, S., T. Hirano, and M. Kamiya. 1969. Seasonal variation in the adjustive responses to sea
water in the intestine and gills of the Japanese
cultured eel, Anguilla japonica. Proc. Jap. Acad.
45:293-297.
Utida, S., T. Hirano, and M. Kamiya. 19726. Response to salinity in teleosts: Mechanisms of ion
and water transport and their hormonal control.
IV Int. Cong. Endocrinol., Washington, D.C. (In
press)
Utida, S., T. Hirano, H. Oide, M. Ando, D. W.
Johnson, and H. A. Bern. 1972a. The role of the
intestine and urinary bladder in teleost osmoregulation. Gen. Comp. Endocrinol. Suppl. 3: 317327.
Utida, S., T. Hirano, M. Oide, M. Kamiya, S. Saisyu,
and H. Oide. 1966. Na+-K* activated adenosinetriphosphatase in gills and deactivated alkaline
phosphatase in intestinal mucosa with special
reference to salt adaptation of eels. Proc. 11th Pac.
Sci. Congr. (Tokyo) 7:5.
Utida, S., N. Isono, and T. Hirano. 1967. Water
movement in isolated intestine of the eel adapted
to fresh water or sea water. Zool. Mag. 76:203-204.
Wikgren, B. 1953. Osmotic regulation in some animals with special reference to temperature. Acta
Zool. 71:1-102.
Zaugg, W. S. 1970. Comments on the relationship
between gill ATPase activities, migration and salt
water adaptation of coho salmon. Trans. Amer.
Fish. Soc. 99:811-813.