Comparative Biochemistry and Physiology Part C 130 Ž2001.

411᎐423

Review
How should salinity influence fish growth? 夽

Gilles Bœuf a,U , Patrick Payan b

a
Laboratoire Arago, Uni¨ ersite´ Pierre et Marie Curier CNRS, BP 44, 66651 Banyuls-sur-mer, France
b
´
UMR Inra-Unsa 1112 ‘Reponses des organismes aux stress en¨ ironnementaux’, Uni¨ ersite´ de Nice-Sophia Antipolis, BP 71,
´ 2, France
06108 Nice cedex

Received 22 December 2000; received in revised form 25 July 2001; accepted 3 September 2001

Abstract

Development and growth Žcontinuous in fish. are controlled by ‘internal factors’ including CNS, endocrinological and
neuroendocrinological systems. Among vertebrates, they also are highly dependent on environmental conditions. Among
other factors, many studies have reported an influence of water salinity on fish development and growth. In most
species, egg fertilization and incubation, yolk sac resorption, early embryogenesis, swimbladder inflation, larval growth
are dependent on salinity. In larger fish, salinity is also a key factor in controlling growth. Do the changes in growth rate,
that depend on salinity, result from an action on: Ž1. standard metabolic rate; Ž2. food intake; Ž3. food conversion;
andror Ž4. hormonal stimulation? Better growth at intermediate salinities Ž8᎐20 psu. is very often, but not systemati-
cally, correlated to a lower standard metabolic rate. Numerous studies have shown that 20 to ) 50% of the total fish
energy budget are dedicated to osmoregulation. However, recent ones indicate that the osmotic cost is not as high
Žroughly 10%. as this. Data are also available in terms of food intake and stimulation of food conversion, which are both
dependent on the environmental salinity. Temperature and salinity have complex interactions. Many hormones are
known to be active in both osmoregulation and growth regulation, e.g. in the control of food intake. All of these factors
are reviewed. As often, multiple causality is likely to be at work and the interactive effects of salinity on physiology and
behaviour must also be taken into account. 䊚 2001 Elsevier Science Inc. All rights reserved.

Keywords: Fish growth; Metabolism; Energetic cost; Osmoregulation; Oxygen consumption; Salinity, Growth hormonal control

1. Introduction environmental factors. Fish are dependent on

Development and growth in teleost fishes take
place following characteristic steps for each
species and more or less directly under control of
夽
This paper was originally presented at a symposium dedi-
cated to the memory of Marcel Florkin, held within the
ESCPB 21st International Congress, Liege, ` Belgium, July
24᎐28, 2000.
U or below Žoxygen. a specific threshold or within a
Corresponding author. Tel.: q33-468-887300; fax: q33-
468-881699.
E-mail address: gboeuf@obs-banyuls.fr ŽG. Bœuf..
both internal Žnervous, endocrinological and neu-
roendocrinological. and external Žecological. fac-
tors, which control or synchronize many activities
or functions, including growth capacity. It is possi-
ble to classify such ecological factors into two
types: Ž1. determining factors Žtemperature, salin-
ity, photoperiod. which act directly through re-
ceptors to increase or decrease growth; and Ž2.
limiting factors, which operate above Žammonia.
tolerance range ŽpH..
In fish, growth is a specific physiological func-

1532-0456r01r$ - see front matter 䊚 2001 Elsevier Science Inc. All rights reserved.
PII: S 1 5 3 2 - 0 4 5 6 Ž 0 1 . 0 0 2 6 8 - X
412 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
tion, which differs from that observed in birds
and mammals. Firstly, growth is continuous, so
that fish become larger the longer they live and
they are much more dependent on external envi-
ronmental conditions ŽBrett, 1979; Bœuf et al.,
1999.. The effects of temperature are obvious in
these ectotherms, but, for instance, light effects
on development and growth were also shown and
recently reviewed ŽBœuf and Le Bail, 1999.. All
these facts must be considered when developing
fish culture ŽBœuf, 2001., which essentially aims
to produce fish of the best quality at the most
economical cost. This requires, when possible,
judicious and careful use of ecological factors to
provide products of consistent quality for the
market during most of the year.
Among the ecological factors, salinity is specific
to the aquatic environment. Many authors have
demonstrated the influence of external salinity on
growth capacities in fish Žsee Table 2.. This is true
for a lot of species, including both marine and
freshwater ŽFW. fish. In fact, species not influ-
enced by salinity changes during their develop-
ment and growth are rare. It is also well known
that many juveniles prefer intermediary salinities,
as found, e.g. in estuaries, tidal coastal areas or
coastal lagoons. In fact, rather than asking: ‘does
salinity have an influence on fish growth?’, a
much better question would be: ‘how should
salinity influence growth?’.
2. Acclimation to salinity and its influence on
growth
Salinity is due to the presence of salts, dis-
solved in water, which represent 60 of the 92
‘basic’ chemical elements ŽRiley, 1965.. Chloride
Cly Ž560 mM. and sodium Naq Ž450 mM. are the
most important in normal salinity sea water ŽSW,
35 psu, 1050 mOsm ly1 .. The global content of 35
psu SW includes 77.8% of NaCl and 10.9% of
MgCl 2 ŽTchernia, 1969.. The most important as-
pect is that these elements are ionised in SW Ž19
g of Cly ly1, 10.5 g of Naq ly1 .. As a comparison,
despite the fact that it is extremely difficult to
specify what an ‘average’ composition of FW re-
ally is, Tchernia in 1969 tried to consider some
data and proposed ‘general values’ for FW Ž0.32
psu., 35.1% of CO 32y, 20.4% of HCOy 3 , 12.1% of
SO42y, 11.7% of SiO 2 and 5.8% of Naq. If chlo-
ride and sodium are predominant in SW, carbo-
nates and HCOy 3 are most abundant in FW. The
composition of FW can vary a lot, but it is impor-
tant to remember that FW is not deionised water!
Many physiological experiments have maintained
fish in deionised water and the fish obviously
rapidly face physiological disturbance, often die
and, if they survive, are unable to grow. Some
species are known for their ability to acclimate to
very different salinity media ŽGriffith, 1974; Jor-
dan et al., 1993; Suresh and Lin, 1992., including
extreme environments Ž) 100 psu.. Killifish
ŽCyprinodontiformes. are particularly interesting
because of their capacities to acclimate to such
environments and represent nice models in bi-
ology. An extreme situation is the persistence of
the Austrofundulus limnaeus population, because
diapausing embryos become embedded in pond
sediments ŽPodrabsky and Hand, 1999..
Osmosensitivity and salinity detection are of
the highest physiological interest. Fish have pro-
lactin ŽPRL. cells which are directly osmosensi-
tive ŽGrau et al., 1994.. They also possess
chemoreceptors, situated in the pseudobranch
ŽLaurent and Dunel-Erb, 1984., providing infor-
mation on water salinity. These are connected to
the central nervous system ŽCNS. and participate
in triggering water drinking in SW. Several hor-
mones are known to be involved in such pheno-
mena, among them the renin᎐angiotensin system
ŽPerrott et al., 1992. and growth hormone GH
ŽFuentes and Eddy, 1997.. Water drinking has
been estimated in both FW and SW Atlantic
salmon Salmo salar ŽFuentes and Eddy, 1997;
Usher et al., 1988.. Drinking rates change from
0.1 to 3.88 ml kgy1 hy1 after transfer from FW to
SW and 10 days after SW contact, they can reach
7.94 ml kgy1 hy1 . Data for several fish species
are shown in Table 1. Teleost fish in SW drink, at
least in part, to compensate for the water lost by
diffusion Žto balance osmotic water losses occur-
ring due to the osmotic difference between their
´
milieu interieur and the external medium., essen-
tially through the gill. Many species have also
developed impermeabilization mechanisms to
avoid too great a loss Žfor review, see Evans, 1975,
1984, 1993; Payan et al., 1984.. Clear evidence for
a relationship between drinking mechanisms and
growth control is not available, but it cannot be
excluded, because such a behaviour has an ener-
getic cost. It can also be presumed that digestive
enzymes are affected by water content in the gut.
The possibility of a direct physical action of salin-
 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
Table 1
To drink in sea water?
Species
Salmo salar ŽAtlantic salmon. FW
SW
Salmo salar 6 h SW
10 d SW
Oncorhynchus mykiss Žrainbow trout.
Scophthalmus maximus Žturbot.
Limanda limanda Ždab.
Pleuronectes platessa Žplaice.
Anguilla anguilla Žeel.
Merlangius merlangus Žwhiting.
Myxocephalus scorpius Žsea scorpion.
Agonus cataphractus Žpogge.
Anarhichas lupus Žwolffish.
Ammodytes lanceolatus Žsand eel.
Data are indicated for different fish species in ml kgy1 hy1 in FW and SW.
ity on digestive enzyme effectiveness remains to
be elucidated.
Many authors have reported on the influence
of water salinity on fish development. In sea bream
Ž Sparus aurata. larvae, growth was estimated at 15
to 40 psu and the best results, in terms of weight
increase and swimbladder inflation, were recorded
at 25 psu ŽTandler et al., 1995.. In greenback
flounder Ž Rhombosolea tapirina., egg fertilization,
incubation and yolk sac resorption are dependent
on salinity, with 28 psu resulting in the best
overall performance ŽHart and Purser, 1995.. In
other flatfish, as the summer flounder Ž Para-
lichthys dentatus . or Southern flounder Ž P.
lethostigma., early development and larval growth
were also affected by salinity, optimal conditions
being 8᎐14 and 5᎐30 psu, respectively ŽSmith et
al., 1999; Specker et al., 1999.. For mulloway
Ž Argyrosomus japonicus. and milkfish Ž Chanos
chanos., yolk resorption, early embryogenesis and
larval growth were optimal at salinities of 5᎐12.5
and 20᎐35 psu ŽFielder and Bardsley, 1999; Swan-
son, 1996.. In striped bass Ž Morone saxatilis.,
growth and yolk sac utilization were optimal at 5
psu, compared with 0 and 10 psu ŽPeterson et al.,
1996.. In the red tilapia Žhybrid Oreochromis
mossambicus= O. urolepis., early development
and growth were optimal at 18 psu Žtested range,
4᎐36 psu. ŽWatanabe et al., 1989.. A change from
0 to 36.6 psu SW did not affect growth in the
tilapia O. spilurus, when the salinity was increased
progressively over 120 h ŽJonassen et al., 1997.. In
the salmonid Oncorhynchus keta Žchum salmon.,
413
Drinking rate Reference
Žml kgy1 hy1 .
0.1 Fuentes and Eddy Ž1997.
3.88
2.4 Usher et al. Ž1988.
7.94
5.38 Shehadeh and Gordon Ž1969.
1.4 Carroll et al. Ž1994.
2.9 Carroll et al. Ž1995.
2.48
1.0 Perrott et al. Ž1992.
1.8 Perrott et al. Ž1992.
7.8 Perrott et al. Ž1992.
2.21 Perrott et al. Ž1992.
2.24 Perrott et al. Ž1992.
2.96 Perrott et al. Ž1992.
increasing the salinity to 33.5 psu during rearing,
following 7 weeks in FW Ž7᎐10 g fish., allowed an
increased growth ŽKojima et al., 1993.. The
metabolic rate of newly hatched steelhead trout
Ž O. mykiss. alevins was significantly lower in 8 psu
water, and higher at 12, in comparison to either 0
or 4 psu ŽMorgan et al., 1992..
In terms of the influence of salinity on the
growing capacities in larger fish, juveniles or
adults, data from numerous studies are available
and these results are summarised in Table 2. In
fact, many fish species have been tested and al-
most always the level of salinity influences growth.
This has been demonstrated for both ‘true’ ma-
rine species Ži.e. cod. or FW species Ži.e. carp..
Studies in tilapias, using salinities between 0 and
120 psu, determined that certain species or hy-
brids have astonishing growth capacities Žre-
viewed in Suresh and Lin, 1992.. Most species
grow optimally between 5 and 18 psu, although
red tilapia prefer 30᎐35 psu. In a seminal paper
ŽWatanabe et al., 1988. on red tilapia, food in-
take, food conversion and growth rates were
closely related with increased salinity up to 36
psu. Analysing the data presented in Table 2, it
appears that a few comments are necessary: all
the results are also dependent on the water tem-
perature. As a consequence, it is extremely im-
portant to take this into account, and to clearly
separate effects between temperature and salin-
ity. For instance, salmonids can grow better in
SW during the winter in net-pen culture, often
independently of the higher salinity, since tem-
414 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423

perature is higher than in rivers during this sea-
son. Also depending on the duration of the exper-
iment, or on the developmental stage of the ani-
mal, results may differ between authors. This was
demonstrated for smoltifying salmonids, where
the smolt status profoundly influenced salinity
‘receptivity’, osmotic capacities and growth ŽBœuf,
1993.. In any case, salinity clearly influences
growth in fish. In experimenting with FW species,
carp Cyprinus carpio, white Amur Ctenopharyngo-
don idella and juvenile Russian sturgeon Acipenser
guldenstaedti, it was shown that a salinity of 2 psu
considerably increased growth rate and food ef-
ficiency, by improving the food conversion rate
ŽKonstantinov and Martynova, 1993.. Moreover,
respiration rate and MO 2 decrease, and fluctua-
tions between 0 and 2 psu are even more effi-
cient. In contrast to this, in ‘true’ SW species,
such as cod Gadus morhua, or turbot Scophthal-
mus maximus, the growth rate is significantly in-
creased at intermediate salinity conditions of
12᎐19 psu ŽLambert et al., 1994; Gaumet et al.,
1995; Dutil et al., 1997; Imsland et al., 2001.. In
cod, an increase in food conversion efficiency
results in a higher growth rate at lower salinity,
whereas turbot increase their food intake
ŽGaumet et al., 1995.. A recent review ŽImsland
et al., 2001. concludes in better growth and better
food efficiency if turbot is reared at intermediate
salinities Ž15᎐19 psu. in the upper temperature
range Ž) 18⬚C.. If fish growth is obviously influ-
enced by the water temperature, salinity interac-
tions also occur.
In conclusion, it appears that marine fish pre-
sent higher developmental or growth rates at
lower salinity and FW fish at higher salinity. Many

Table 2
Salinity and growth

Species Tolerance Best growth Reference

Pomatomus saltatrix ŽBluefish. s Ž5 and 25 psu. Buckel et al. Ž1995.

Micropogonias furnieri ŽCroaker. qŽ10᎐30. 17᎐19 Aristizabal Abud Ž1992.
Sparus sarba ŽSea bream. qŽ0᎐35. 15 Woo and Kelly Ž1995.
Oreochromis niloticus ŽTilapia. qŽ0᎐16. 8 Likongwe et al. Ž1996.
Oreochromis spilurus Tilapia s Ž0᎐37. Jonassen et al. Ž1997.
Oreochromis aureus ŽTilapia. s Ž0᎐27. Chervinsky and Yashouv Ž1971.
O. mossambicus ŽTilapia. 120 psu 17.5 Suresh and Lin Ž1992.
O. niloticus ŽTilapia. 36 5᎐10 Suresh and Lin Ž1992.
O. aureus ŽTilapia. 40 10᎐15 Suresh and Lin Ž1992.
O. spilurus ŽTilapia. 36 0 Suresh and Lin Ž1992.
Hybrid Red ŽTilapia. 35 30᎐35 Suresh and Lin Ž1992.
Morone chrysops ŽWhite bass. q0᎐20 psu 0᎐12 Heyward et al. Ž1995.
Chanos chanos ŽMilkfish. q0᎐55 55 Swanson Ž1998.
Chanos chanos ŽMilkfish. q0᎐35 0 Alava Ž1998.
Trinectes maculatus ŽHogchoker. q0᎐30 30 Peters and Boyd Ž1972.
Trinectes maculatus ŽHogchoker. q0᎐15 Peterson-Curtis Ž1997.
Gadus morhua ŽCod. q14 and 28 psu 14 Dutil et al. Ž1997.
Mugil sp. ŽMullet. q3᎐24 17 Peterson et al. Ž1999b.
Chelon labrosus ŽGrey mullet. s Ž5᎐25. ´
Cardona and Castello-Orvay Ž1997.
Salaria flu¨ iatilis ŽBlenny. q0᎐35 12 Plaut Ž1999.
Micropogonias undulatus ŽAtlantic croaker. q0᎐20 5 Peterson et al. Ž1999a.
Sparus aurata ŽGilthead seabream. q8᎐38 28 Conides et al. Ž1997.
Dicentrarchus labrax ŽEuropean seabass . q0᎐35 10᎐35 Bœuf et al. Žunpublished.
Lutjanus argenti¨ entris ŽAmarillo snapper. q3᎐24 psu 30 ˜
Serrano-Pinto and Caravea-Patino
Ž1990.
Salmo salar ŽAtlantic salmon. q0᎐35 22᎐28 Bœuf et al. Žunpublished.
Oncorhynchus mykiss ŽRainbow trout. s Ž0 and 34. Bœuf et al. Žunpublished.
Oncorhynchus mykiss ŽRainbow trout. qŽ0᎐16. 0 Morgan and Iwama Ž1991.
Oncorhynchus keta ŽCoho salmon. q0᎐35 22᎐28 Bœuf et al. Žunpublished.
Sal¨ elinus alpinus ŽArctic charr. q0᎐35 0᎐20 Arnesen et al. Ž1993.
Scophthalmus maximus ŽTurbot. q0᎐35 10᎐19 Gaumet et al. Ž1995.

The influence of salinity on growth of different species of fish are indicated as follows: Žpositive q, or neutral s., tolerance
Žmaximum salinity or range tested., the best salinity conditions for growth, and the reference.
 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
species, often as juveniles, opt for intermediary
salinity conditions of the brackish water Ž8᎐16
psu. and grow optimally in estuaries and costal
systems.
3. Discussion
From all these data, several questions arise. At
high, intermediate or low salinity, does higher
growth rate in fish result from: Ž1. a lower stan-
dard metabolic rate? Ž2. an increased food in-
take? Ž3. an increased protein digestibility Žbetter
food conversion.? or Ž4. an hormonal stimula-
tion?
3.1. Energetic cost
The overall picture of osmotic regulation for
both FW and SW fish species is reasonably clear
since osmoregulatory organs and tissues have been
identified Ždigestive tract, gill, kidney, urinary
bladder and liver in ureotelic regulators.. Both
passive and active fluxes of solutes Žmainly NaCl
plus urea in ureotelics. have been estimated in
many species. The question is how much MO 2 is
specifically dedicated to the hydromineral balance
regulation? Two major approaches have been
used: Ž1. the classical approach, based on the
direct measurement of O 2 consumption either in
whole fish or in individual tissues; and Ž2. the
molecular approach based on ATPrO2 consump-
tion by ionic fluxes andror urea synthesis in-
volved in osmoregulatory patterns.
As for Ž1., the difference obtained by substract-
ing total metabolic rate in fish held in isotonic
conditions from the rate measured in a non-iso-
tonic situation has usually been attributed to the
extra cost of osmoregulation ŽParry, 1966.. In the
optimally designed metabolic studies, fish were
made to swim at different speeds in FW, isotonic
medium and SW and MO 2 was measured at each
speed ŽRao, 1968; Farmer and Beamish, 1969;
Febry and Lutz, 1987.. Fish in an isotonic medium
had the lowest standard metabolic rates, whereas
osmoregulation in SW appeared to be energeti-
cally more expensive than in FW, as might be
expected from the NaCl gradient between milieu
´
interieur and external medium. There are con-
flicting reports in the literature ŽMorgan and
Iwama, 1991. regarding the effects of isotonic
salinity Ži.e. 9᎐12 psu; Brett, 1979. on the
415
metabolic rate and growth of fish. Several authors
ŽCanagaratman, 1959; Otto, 1971. found that
growth rates of pre-smolts of coho salmon O.
kisutch were higher between 5 and 12 psu than in
FW. MO 2 measurements in rainbow trout O.
mykiss also showed a drastic reduction in
metabolic rate Ž20᎐28%. at an isotonic salinity
relative to that in FW andror SW ŽRao, 1968..
Such studies support the hypothesis that the ener-
getic cost of osmoregulation is lower in an isos-
motic medium, where the gradients between blood
and water are minimal, and that these energy
savings are substantial enough to increase growth.
For instance, it was estimated that osmoregula-
tion might consume as much as 54᎐68% of the
non-swimming metabolic output in two species of
tunas ŽBushnell and Brill, 1992.. Even in species
with lower metabolic rates, osmoregulation ap-
pears to use a high proportion of the available
energy, ranging from 20 to ) 50% of the total
energy expenditure Žroughly 100᎐150 ml hy1 kgy1
O 2 . dependent on the environmental salinity
ŽRao, 1968; Nordlie and Lefler, 1975; Nordlie,
1978; Furspan et al., 1984; Nordlie et al., 1991;
Toepfer and Barton, 1992., for rainbow trout,
Mugil cephalus, catfishes Ictlalurus punctatus and
I. Žnow: Ameiurus. nebulosus, Cyprinodon ¨ ariega-
tus, minnow Phoxinus erythrogaster and killifish
Fundulus catenulatus, respectively. Theoretically,
a gill ideally designed to absorb oxygen for the
energetic requirements, should be highly perme-
able with a rather large surface area leading to an
ascending metabolic cost of osmoregulation ŽGrau
et al., 1994.. These conflicting demands may rep-
resent the major constraint in the overall
metabolic capacity of teleostean fish. All fish ap-
pear to be limited by the need for an ‘osmoregu-
latory compromise’ ŽNilsson, 1986.. The energetic
cost of ionic regulation increases with alteration
of the salinity away from iso-osmotic conditions,
but any attempt to quantify this cost is probably
affected by other metabolic processes which re-
spond to changes in salinity ŽMorgan and Iwama,
1991..
As for Ž2., a totally different approach was
elaborated and proposed more recently
ŽKirschner, 1993, 1995.. It takes advantage of the
fact that: Ž1. a central process in osmotic regula-
tion is active Naq transport; Ž2. a great deal of
energy is consumed in moving ions through a
Naq᎐Kq-pump on the basolateral side of the
transporting epithelia; and Ž3. the ratio of Naq
416 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
transported to ATP consumed in this process is
generally known for most transport epithelia.
Table 3 summarizes the oxygen consumption ded-
icated to osmoregulation by the regulatory organs
Žintestine and gill in SW teleosts, kidney and gill
in FW teleosts and kidney, liver and rectal gland
in SW ureotelic elasmobranchs .. The values for
the energetic cost generated by this methodology
are considerably lower than those obtained by
measuring direct O 2 consumption Žafter changes
from isotonic water to FW or SW. and represent
approximately 10% of the total standard
metabolic in SW and much less in FW. It would
be possible to also take into account the cost of
Cly extrusion through the gill, involving for in-
stance CFTR ŽMarshall et al., 1999; Chen et al.,
2001.. In Fig. 1, the total oxygen consumption was
plotted against the osmotic gradient between in-
ternal and external medium Žy700 for teleosts in
SW, 0 in elasmobranchs and q300 mOsm ly1 in
teleosts in FW.. It appears that the estimated
energy demands of the two modes of osmotic
regulation in SW are indistinguishable. This is a
surprising fact because marine teleosts need to
cope both with water loss and salt entry, whereas
elasmobranchs have eliminated the osmotic gradi-
ent by using the ureotelic system. In these mod-
els, rectal gland energetics, as those in renal urea
absorption play a minor role. It is clear that the
major part of the cost of ureotelic regulation is
linked with urea synthesis which involves an en-
ergy-dependent process Ž5 ATP per molecule of
urea synthesised, via the ornithine cycle.. It might
be worth pointing out that in ureotelic organisms
while urea is especially synthesised for osmoregu-
lation, a proportion is made by normal metabolic
processes anyway. The question is how significant
this is compared with additional syntheses. In a
recent study, it is specified that the energetic cost
of NaCl transport Žin cutthroat trout O. clarki . in
Table 3
Oxygen consumption Žml kgy1 hy1 . dedicated to osmoregulation Ždata from Kirschner, 1993, 1995; Morgan, 1998.
Osmoregulatory Salmon Flounder
organs SW SW
Intestine 1.4 3.1
Gill 4.3 4 1.05
Kidney
Rectal gland
Liver
Total 5.7 7.1
FW and SW gills represents a relatively small
Ž- 4%. portion of the animal’s total energy bud-
get ŽMorgan and Iwama, 1999.. However, it is
important to consider potential problems posed
by only using Naq flux data to calculate associ-
ated ATP usage. For instance, is Na transport
100% efficient? The gill NaCl transport by chlo-
ride cells Žmitochondria-rich cells. is not totally
known. As Naq ions are not thought to be di-
rectly and exclusively excreted by Naq᎐Kq-
ATPase, but rather via the basolateral tubular
network, either through diffusion or an active
bulk flow mechanism, the energy required could
be underestimated. Many of the ions transported
by ATPases may simply diffuse back out the ba-
solateral network into body fluids, or if the bulk
flow hypothesis is correct, the energy to drive this
would also need to be estimated. There are also
potential difficulties in measuring Naq transport
in isolated gills. It is quite difficult to be sure that
one has an accurate estimate of sodium transport
and any error, such as difficulties with full perfu-
sion are likely to reduce the estimates produced.
Even inhibitors such as ouabain or basilomycin
may also affect the perfusion, as well as Naq
transport. In addition, changing cellular Naq gra-
dients during experiments could also have knock-
on effects on other cellular metabolic processes.
Thus, even if such experiments allow new ideas,
we have to remain careful. But, if osmoregulation
mechanisms, even in the case of SW teleosts, are
not as expensive in terms of energy expenditure,
howrwhy does salinity affect growth?
3.2. Food intake andr or food con¨ ersion
stimulation
Experiments with cod Ž G. morhua., demon-
strated that growth was higher at 7 psu salinity
than in SW Ž28 psu. during the spring ŽLambert
Dogfish Skate Trout
SW SW FW
0.27 0.15 0.6
0.03 0.19
4.7 11 Ž4.6.
5 11.3 Ž4.9. 1.65
 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
Fig. 1. Energetic cost of osmoregulation in fish. The osmotic gradient indicates the difference between the Milieu interieur Žfish. and
the external medium.
et al., 1994.: better growth rates at lower salinity
conditions resulted from an increase in food con-
version efficiency. It was not associated with an
increase in food intake, changes in composition
Žproteins, lipids, water. or relative allocation of
energy to the tissues Žmuscle, liver and gonads..
In a more recent experiment with the same
species, the best growth was found at 14 psu, and
protein digestibility was not related to salinity
ŽDutil et al., 1997.. Higher growth rates and bet-
ter food conversion ratios were attributable to
uncontrolled or unmeasured factors such as spon-
taneous activity and swimming performance
rather than to changes in standard metabolic rate
or protein digestibility. In another marine species,
the turbot, growth rate was also better at 10᎐19
psu, in comparison to fish in full strength SW Ž34
psu, 17⬚C.. However, this fact appears to be linked
directly to the food ingestion ratio ŽGaumet et al.,
1995.: turbot eat more at lower salinity at this
temperature. However, in a recent review, Ims-
land et al. Ž2001. indicate that it is more complex
and that temperaturersalinity interactions hap-
pen. At any rate, such a behaviour is finally very
417
´
common: in many studies where fish are exposed
to different environmental conditions Žtempera-
ture, light, salinity, hypoxia, etc.. and if changes in
growth rates are observed, it is often because fish
control food intake ŽLe Bail and Bœuf, 1997..
This leads us to the next section: which hormones
regulate food intake in fish?
3.3. Hormonal stimulation
Several reviews have pointed out the involve-
ment of hormones in osmoregulation ŽJohnson,
1973; Madsen, 1990; Madsen and Bern, 1992;
Bern and Madsen, 1992; Sakamoto et al., 1993,
1997; McCormick, 1994, 1996; Balm et al., 1995;
Seidelin and Madsen, 1997. and in growth
ŽDonaldson et al., 1979; Weatherley and Gill,
1987; Duan and Hirano, 1992; Bœuf, 1993; Duan
et al., 1995; Bœuf and Le Bail, 1999.. From Table
4, it appears that several hormones are known to
be involved in both osmoregulation, and growth
control and regulation. There is a specific situa-
tion where growth and SW tolerance, i.e. eury-
halinity acquisition Žand, by extension osmoregu-
418 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
Table 4
Hormones and osmoregulation Ždata from Bern and Madsen,
1992; Bœuf, 1993; Sakamoto et al., 1993.
Pituitary role Others
Growth hormone, IGF1 and PRL Stannius corpuscles
ACTH and cortisol Endocrine kidney
TSH and thyroid hormones, T3 , T4 Chromaffin tissue
GtHs and androgens or estrogens Calcitonin
NeurohypophysisrAVT Urophysisrurotensin
AtriumrANP
Interrenal and thyroid
latory capacities., are closely linked: e.g. the
parr-smolt transformation in salmonids ŽBœuf,
1993.. Critical situations were demonstrated
where growth is stopped, because osmoregulation
is not totally controlled: the stunting pheno-
menon in coho salmon, for instance. Under such
severe conditions, the fish can survive, but only by
enduring a chronic osmotic disequilibrium, and
cannot grow after transfer to SW, although a
return to FW allows the fish to resume immediate
growth ŽYoung et al., 1989.. In these stunted coho
salmon, blood plasma levels of GH are very high,
while thyroid hormone levels are very low and
IGF1 production is arrested ŽYoung et al., 1989;
Gray et al., 1990.. In fact, there is no GH recep-
tivity. Salmonid smoltification represents a very
interesting model in studying hormones involved
in both osmoregulation and growth ŽBœuf, 1993.,
and optimal salinities for growth and metabolic
rates are influenced both by species and develop-
mental status ŽMorgan and Iwama, 1991..
GH level is temporarily increased by SW trans-
fer in salmonids ŽBœuf et al., 1989; Rydevik et al.,
¨
1990; Bœuf, 1993; Bjornsson, ¨
1997; Bjornsson et
al., 1998.. This hormone, obviously involved in
growth control, is also very active in the hypo-
osmoregulatory performance of several species in
SW ŽSakamoto et al., 1993, 1997; Bœuf et al.,
¨
1994; Borski et al., 1994; Bjornsson et al., 1995;
Mancera et al., 1995.. In fact, the somatotropic
axis Žincluding GH, GH-Receptor ŽR., IGF1,
IGF1-R. is a major regulator of both growth and
SW acclimation ŽMcCormick, 1994, 1996;
Mancera and McCormick, 1998..
In addition, opposing effects of 17␤-estradiol
compared to GH on osmoregulatory capacities
have been recorded ŽMadsen and Korsgaard,
1991.. Cortisol is also a very active hormone in
osmoregulatory processes in SW ŽMadsen, 1990;
Franklin et al., 1992; Hwang and Wu, 1993; Balm
et al., 1995., but without any clear influence in
terms of growth capacity control. No information
is available about a possible role in growth by
means of other types of osmoregulatory hor-
mones, as for instance, atrial natriuretic peptide
ŽAndo et al., 1992. or corpuscles of Stannius
hormones ŽButler, 1999.. However, thyroid hor-
mones ŽTH, T3 and T4 . are clearly involved in
growth regulation in fish and also in osmoregula-
tory capabilities in several species ŽKnoepel et al.,
1982; Parker and Specker, 1990.. However, this
osmoregulatory action is less obvious in sal-
monids ŽBœuf, 1993.. The other hormone with a
major involvement in osmoregulation in fish is
PRL ŽPrunet et al., 1990; Madsen and Bern, 1992;
Bole-Feysot et al., 1998.. PRL appears to act as a
‘key-hormone’ for osmoregulatory capabilities in
FW fish. PRL appears as an antagonist to GH
during SW acclimation ŽMadsen and Bern, 1992;
Seidelin and Madsen, 1997., but has never been
proposed as acting on growth in fish.
The somatotropic axis is the majority system in
controlling growth in fish. It also plays a de-
termining role in osmotic capacities in SW. This
is probably why, in many situations, salinity adap-
tation may be linked to stimulated growth.
4. Conclusion
In fish, often Žin fact, almost always. a better
growth rate is observed in intermediary salinity
conditions, i.e. in brackish water Ž8᎐20 psu.. This
is often, but not systematically, correlated with a
lower standard metabolic rate. Specific experi-
ments, designed to demonstrate this fact did not
succeed each time ŽMorgan and Iwama, 1991;
Swanson, 1998; Plaut, 1999.. Recent experiments
indicate that the true energetic cost of osmoregu-
lation remains under debate, ranging from 20 to
) 50% of total energy budget in several studies
to 10% in more recent times ŽKirschner, 1993;
Morgan and Iwama, 1999.. So different results
are worth discussing. For one thing, it might be
worth asking what explanations there might be to
understand why fish are estimated to use up to
50% of energy for osmoregulatory purposes using
measurements of the overall metabolic rates in
non iso-osmotic conditions compared with figures
as low as a few percent in studies more directly
measuring the energetics of Na transport. What
 G. Bœuf, P. Payan r Comparati¨ e Biochemistry and Physiology Part C 130 (2001) 411᎐423
possible ‘metabolic’ factors might change so radi-
cally between say iso-osmotic conditions and sea-
water Žwith an associated change in plasma os-
molality of 20᎐40 mOsm ly1 . that might explain
such a discrepancy? Interactive effects of salinity
on physiology and behaviour have to be taken
into account: tissue permeabilities to water and
ions, gill ventilation, perfusion, functional surface
area, types of metabolic substrates catabolized,
among others ŽSwanson, 1998..
Many indications suggest that better growth in
brackish water would depend on controlled food
intake because many species adapt food ingestion
to the external water salinity. Such a behaviour of
course is under the control of the CNS and sev-
eral hormones including insulin, glucagon,
adrenalin, CCK, PYY, GH, TH ŽLe Bail and
Bœuf, 1997.. Several results have been obtained
in terms of better food conversion efficiency,
however, mechanisms for explaining this are still
questionable Žprobably not better protein di-
gestibility.. Finally, several hormones ŽTH, GH,
IGF1, among others., clearly involved in growth
control, are also active in osmoregulatory
processes and may play a determining role in
both osmoregulation and growth. Growth and
food conversion are influenced by both tempera-
ture and salinity and complex interactions appear
ŽImsland et al., 2001.. Elevation of plasma sodium
levels due to increases in external salinity may
also have cellular effects on growth. Increases in
intracellular sodium, sometimes occuring in some
species or according to salinity changes, are known
to be mitogenic and this may be another factor
which could potentially contribute to changes in
growth rates in specific situations. Further experi-
ments are needed to clarify the situation but, as
so often in biology, multiple causality is likely to
be at work. With regards to each possibility and
proposed hypothesis, the CNS and related en-
docrinological and neuroendocrinological systems
represent the key to explain such relationships
between salinity adaptation mechanisms and de-
velopmental and growth capacity in fish.
Acknowledgements
The authors wish to thank S. Von Boletsky and
an anonymous reviewer for their help in improv-
ing the quality of the English language, I. Vallde-
perez for typing of the references and S. Maria
419
and M.T. Panouse for their help in bibliographi-
cal data search. One anonymous reviewer pro-
vided many constructive comments.
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