Directory UMM :Data Elmu:jurnal:J-a:Journal of Experimental Marine Biology and Ecology:Vol244.Issue2.Feb2000:
Journal of Experimental Marine Biology and Ecology
244 (2000) 253–263
L
www.elsevier.nl / locate / jembe
Effect of salinity in survival, growth, and osmotic capacity
of early juveniles of Farfantepenaeus brasiliensis (decapoda:
penaeidae)
´
Roberto Brito a , Marıa-Eugenia
Chimal b , *, Carlos Rosas b
b
a
Center of Marine Research, Havana University, Havana, Cuba
Group of Experimental Marine Biology, Laboratory of Ecophysiology, Faculty of Sciences,
UNAM. Apdo. Post. 69, Ciudad del Carmen, Campeche, Mexico
Received 15 May 1999; received in revised form 26 June 1999; accepted 22 September 1999
Abstract
The effect of salinity in survival, growth and osmotic capacity of juvenile Farfantepenaeus
brasiliensis was determined. Survival was not affected by salinities from 15 to 35‰ during 96 h
exposure periods. Shrimps exposed to 5 and 10‰ were noticeably affected by salinity with a
survival of 0 and 48% after 96 h, respectively. Lethal salinity for 50% of the individuals in 96 h
(LS 50 , 96 h) at 288C was 10‰. Growth rate (mg dw day 21 ) was significantly higher at higher
salinities. The isosmotic point of early juvenile F. brasiliensis was 794 mOSm kg 21 , at around
25‰. Results indicate that F. brasiliensis has low tolerance to low saline environments, and grows
better in salinities greater than its isosmotic point. Osmotic capacity seemed to be related to
biological characteristics that determine the environmental preferences and behavior, as well as the
distribution of this shrimp species. 2000 Elsevier Science B.V. All rights reserved.
1. Introduction
Increased interest in the physiology of penaeid shrimp has derived from
the aquaculture industry in many regions of the world. Many studies have focused on
he biological aspects of several shrimp species, and increasing knowledge in this
research field has allowed optimal conditions for their culture. For Farfantepenaeus
brasiliensis, not much information of the biology is known, although it is distrib-
*Corresponding author.
0022-0981 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved.
PII: S0022-0981( 99 )00142-2
254
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
uted along the Florida coast in USA to the Bermudas and the Antilles, and along
the Atlantic coast of South America to Rio Grande do Norte, Brazil (Sandoval,
1996).
In Mexico, F. brasiliensis has great economic importance in the fishery around the
Peninsula of Yucatan. In this region, red shrimp are caught all year, mainly in the
´ ´
northwest of the Isla Contoy (Arreguın-Sanchez,
1981) and in a lesser amount in the
Gulf of Mexico toward Cabo Catoche (Silva Neto et al., 1982).
Little is known about this species, the present information is mainly on its distribution
and fishery. Biological and physiological aspects are virtually unknown; hence the need
to do research that contributes to the knowledge of the environmental requirements of F.
brasiliensis and to help establish a basis for its culture. To date, there are no studies that
approach, in any integral way, the effects of salinity on the physiology of this shrimp
species.
Postlarvae and juveniles are exposed to salinity, temperature, dissolved oxygen, and
pH changes characteristic of coastal environments. Numerous investigations have
demonstrated that when juveniles are exposed to environmental changes, there are
modifications in the ionic and osmotic balance (Dall and Smith, 1981; Castille and
Lawrence, 1981; Rosas et al., 1999a), respiratory activity (Dalla Via, 1986; Kutty et al.,
1971; Rosas et al., 1999a; Chen and Nan, 1995), assimilation and growth (Chen et al.,
1992; Ogle et al., 1992; Bray et al., 1994; Rosas et al., 1999b), and ammonia excretion
(Spaargaren et al., 1982; Chen and Lai, 1993; Chen and Nan, 1995). These results have
provided evidence that penaeid shrimp are well adapted to tolerate environmental
fluctuations.
According to Castille and Lawrence (1981), and Claybrook (1983), the adaptive
capacity of penaeid shrimps is specific and is determined by a number of evolutionary
factors that have caused shrimp species to be distributed differently in the estuarinemarine gradient. F. brasiliensis have been associated with a high saline environment
´˜
from north of Brazil to the Caribbean Sea (Scelzo and Zuniga,
1987; Sandoval, 1996).
For that reason, F. brasiliensis may be identified as have been F. aztecus and F.
duorarum as limited euryhaline shrimp species (Zein-Eldin and Renaud, 1986; Wenner
and Beatty, 1993). In that sense, (Venkataramiah et al., 1974) showed that such
characteristic could be related with limitation on physiological mechanisms associated
with the osmotic balance, which affect the energetic metabolism, the osmotic pressure,
and finally the growth. On this base is possible to think that limited capacity for osmotic
regulation of F. brasiliensis could be associated with the natural range distribution of
this species.
Osmotic capacity (OC) is a useful indicator to measure the stress of shrimp exposed
to a diversity of environmental factors, among them dissolved oxygen (Charmantier et
al., 1994; Rosas et al., 1999a) and pollutants (Lignot et al., 1997). Unpublished data
from studies in our laboratory have demonstrated that coupled to nitrogen excretion,
hemolymph glucose, and hepatopancreas glycogen levels, OC allow us to determine
optimum conditions for growth when shrimp are fed diets with different carbohydrate
levels. The objective of this study was to determine the effect of salinity on growth,
survival, and osmotic capacity of juvenile F. brasiliensis.
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
255
2. Material and methods
2.1. Origin of the animals
The postlarvae and early juveniles of Farfantepeneus brasiliensis used in the
experiments were bred in the Group of Experimental Marine Biology, Faculty of
Sciences, UNAM, in Ciudad del Carmen, Campeche, from spawners captured along the
coasts of Quintana Roo, Mexico. Larvae from naupli I to postlarva 27 (PL 27 , 27 days
after the last metamorphic molt) were maintained in a fiberglass tank of 400 l capacity,
at 37‰ salinity, constant aeration, and pH . 8. Larvae were fed a mixture of unicellular
algae (diatoms and flagellates) and freshly hatched artemia nauplii to PL 5 (Gallardo et
al., 1995). At PL 6 , shrimp were fed a mixture of artemia nauplii (25%) and balanced
food (75%) with 50% protein at 120% of body weight.
2.2. Tolerance to abrupt salinity changes
To determine survival rate, shrimp at PL 28 were transferred without previous
acclimatization from rearing salinity (37‰) to water at 5, 10, 15, 20, 25, 30, and 35‰.
Ten postlarvae in each salinity treatment (three replicates per treatment) were placed in
5 l plastic containers, and the postlarvae surviving after 96 h counted.
Water in each treatment was prepared the day before the experiments by diluting
filtered (5 mm) and ultraviolet sterilized seawater with commercial purified water. The
salinity was determined using an Atago refractometer with 61‰ precision. Organisms
were maintained under controlled experimental conditions of temperature (288C),
photoperiod (12 h:12 h, light: dark) with lighting between 280 and 650 lux, and constant
aeration. Shrimp were fed pellet food G-GAX (Gaxiola, 1994) with 50% protein and
with particle size between 210 and 300 mm at 20% of body weight, and with freshly
hatched artemia nauplii. Shrimp were fed two times daily at 1000 and 1800 throughout
the experiments. Daily water exchange was 50% in all the experimental tanks, with
feces, sheds, and remaining food being withdrawn from all containers. The absence of
movement and absence of response to touch were the criteria for death. Surviving
shrimp were counted at 0.5, 1, 2, 4, 6, 8, 12, 24, 36, 48, 72, and 96 h of exposure in each
treatment. Dead shrimp were removed at time of each observation.
2.3. Osmotic pressure
Early juvenile F. brasiliensis (248616 mg ww) were transferred directly from 37‰ to
salinities of 5, 10, 15, 20, 25, 30, 35, and 40‰ at a temperature of 288C. After 2 h in
these conditions, shrimp were dried on absorbent paper and samples of hemolymph (20
ml from one to three individuals) were taken using a hypodermic needle inserted in the
heart (n between 7 and 17 samples). Osmotic pressure of three water samples in each
treatment was also measured. To measure the osmotic pressure, a microosmometer (3
MO Plus, Advanced Instruments, Inc., Norwood, Massachusetts, USA) was used. Only
shrimp in the intermolt stage were used for these determinations.
256
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
2.4. Growth and survival in different salinities
Before the experiments, a group of 40 individuals was randomly selected, dried on
absorbent paper, and weighed on an OHAUS analytical balance (60.0001 g) to obtain
their initial wet weight. Thereafter, individuals were dried in a stove at 608C for 24 h
and were weighed to obtain the dry weight.
The effect of the salinity on growth and survival of shrimp was studied in animals
acclimated to three salinities; 15, 25 and 35‰. Sixteen PL 34 were placed in 30L plastic
tanks, which were used in each treatment (one replicate per treatment). Shrimp used in
15 and 25‰ salinities were acclimated through a device that supplies tap water to the
experimental tanks until the required salinity was obtained (48 h). However, those
treated at 35‰ were transferred directly from seawater of 37‰.
Shrimp were maintained for 60 days at constant temperature (288C), with a
photoperiod of 12 h: 12 h, light: dark, and constant aeration. Shrimp were fed two times
a day (pellets G-GAX, 50% protein) at 20% of body weight. Daily water exchange was
50% in all the experimental tanks. Feces, sheds, and the remaining food were eliminated
every day during water exchange. Surviving shrimp were counted and temperature, pH,
and dissolved oxygen were recorded on a daily basis. At the end of the experiment,
shrimp were dried and weighed as described previously.
Differences in osmotic pressure, final weight, and growth rate between treatments
were analyzed by one-way analysis of variance. When significant differences were
found, Duncan’s Multiple Range test was used to identify significant differences
between treatments. Differences are reported as statistically significant when P , 0.05
(Zar, 1984). The program STATISTICA 4.5 was used for statistic analysis.
3. Results
3.1. Tolerance to abrupt salinity changes
Survival of postlarval F. brasiliensis was not affected by salinities between 15 and
35‰ during 96 h exposure (Fig. 1). By contrast, shrimps at 10 and 5‰ were affected by
salinity with survival of 48 and 0%, respectively, after 96 h. Lethal salinity LS 50 for 96
h was 10‰ (Fig. 1).
3.2. Osmotic pressure ( OP)
The isosmotic point of early juvenile F. brasiliensis (248616 mg ww) was found
around 25‰ (794 mOsm kg 21 ), a salinity under which the animals were hyperosmotic.
The highest OP was recorded in shrimp at 35‰ (872 mOsm kg 21 ), and it was
significantly different from the OP in 25‰, 40‰, 15–20–30‰, 10‰ and 5‰ salinities
(P , 0.05). The OP of shrimp at 35‰ was 2.3 times that at 5‰ (Table 1) (P , 0.05).
There was found a significant linear relation between medium and hemolymph osmotic
pressure with a slope value of 0.33 (r 2 5 0.68, F 5 12.80, P 5 0.01).
The osmoregulatory capacity (OC) of early juvenile F. brasiliensis varied with
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
Fig. 1. F. brasiliensis (PL
28
257
) survival in different salinities.
salinity. The hypo-OC of shrimp at 40‰ (2421 mOsm kg 21 ) was 2.3 times greater than
that in animals at 30 and 35‰ (average of 2 180 mOsm kg 21 ) (P , 0.05). The lowest
hyper-OC was observed in shrimp at 25‰ (40 mOsm kg 21 ), and increased with
decreasing salinity until it reached its maximum value in shrimp at 10‰ (287 mOsm
kg 21 ). The hyper-OC of animals at 5‰ (251 mOsm kg 21 ) was similar to that in shrimp
at 15‰ (246 mOsm kg 21 ). Fig. 2 shown the OC for several penaeid species, comparing
the OC in extreme salinities, we can separate F. brasiliensis with the highest hypo-OC
from F. chinensis and L. stilyrrostris, when analyzing the hyper-OC, F. brasiliensis and
M. japonicus have the lowest values and L. stylirrostris and L. setiferus the highest
values.
3.3. Growth and survival in different salinity treatments
During growth experiments, water temperature was maintained at 2860.58C, pH
Table 1
F. brasiliensis juveniles and culture water osmotic pressure (mOsm kg 21 ) in different salinities a
Salinity
(‰)
5
10
15
20
25
30
35
40
Shrimp
n
Mean
S.E.
14
380 ( f )
13.9
14
603 (e)
8.1
10
733 (d )
11.5
14
714 (d )
4.9
7
833 ( b)
9.1
11
737 (d )
11.0
17
872 (a)
10.1
13
798 (c)
13.8
Water
n
Mean
S.E.
3
186
1.4
3
307
0.6
3
487
0.5
3
598
3.0
3
794
1.4
3
905
1.2
3
1071
2.8
3
1219
1.2
a
Different letters mean statistical differences (P , 0.05).
F ( p)
179.4
( , 0.001)
258
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
Fig. 2. Osmoregulatory capacity of several shrimp species exposed to salinity changes. F. chinensis (–h–,
Charmantier-Daures et al., 1988), L. vannamei (–m–, Charmantier et al., 1994), L. stylirostris (–♦–,
Charmantier and Aquacop, pers. comm.), M. japonicus (– 3 –, Charmantier et al., 1988), L. setiferus (–j–,
Rosas et al., 1999a), F. brasiliensis (–d–, this paper).
varied between 8.00260.106 in 15‰ and 8.17860.100 in 35‰. Dissolved oxygen was
kept close to the saturation level, varying from 6.9560.20 in 15‰ to 6.2860.15 mgO 2
l 21 in 35‰ salinity. Final body weights and growth rates (mg dw day 21 ) were
significantly greater in shrimp maintained at 35‰ (P , 0.05) (Table 2). Tissue water
content was not affected by the different treatments. For 62 to 64 days, salinity did not
affect the survival of shrimp maintained in any of the three experimental salinities
(93.8% survival) (Table 2).
Table 2
Growth rate (mg day 21 ), body water (%), and survival (%) of F. brasiliensis in different salinities.
Mean6S.E.a
SALINITY ‰
Initial wet weight, mg
Initial dry weight, mg
n
Final wet weight, mg
Final dry weight, mg
n
Days of culture
Growth rate, mg dw day 21
Body water, %
Survival, %
a
15
25
35
21061.1
4.7960.2
41
500621 b
12765 b
12
62
1.9860.09 b
74.560.4
93.8
21061.1
4.7960.2
41
462632 b
122611 b
7
63
1.8760.18 b
73.760.9
93.8
21061.1
4.7960.2
41
568623 a
15166 a
11
64
2.3060.09 a
73.260.06
93.8
Different letters mean statistical differences (P , 0.05).
F (P)
4.25 (0.02)
4.46 (0.02)
3.61 (0.04)
1.27 (0.29)
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
259
4. Discussion
Postlarval (PL 28 ) F. brasiliensis showed a wide range of tolerance to salinity changes,
which closely corresponds with the adaptive mechanisms in penaeids that, at this stage
of their life cycle, inhabit estuarine zones and are exposed to variable salinity. Postlarval
F. brasiliensis grow in coastal lagoons or estuaries for 2 to 4 months before they migrate
into the marine environment for reproduction (Sandoval, 1996).
Lethal salinity for 50% of the animals (LS 50 ) varies among species and depends on
the temperature and developmental stages of the organisms under study. CharmantierDaures et al. (1988) found that in Marsupenaeus japonicus PL 20 – 60 the SL 50 decreased
with increasing temperature, whereas in Fenneropenaeus chinensis, a relation between
SL 50 and temperature did not appear to be so direct, and PL 60 was more resistant to
salinity changes than PL 20 . L. vannamei increases its resistance to salinity changes as
increasing postlarval development (Aquacop et al., 1991; Ogle et al., 1992; Samocha et
al., 1998). In M. japonicus, the 24 h LS 50 at 258C decreased from larval stages to PL 10
stage (Charmantier et al., 1988), corresponding to migrations from the marine ambient
to the estuarine nursery areas that occur during these stages. LS 50 at 288C in PL 28 F.
brasiliensis obtained in the present study was found at 10‰, which was similar to those
reported for PL 40 – 60 for F. chinensis at 258C (10.2–10.5‰) (Charmantier-Daures et al.,
1988) and greater than that found for PL 10 – 21 stages of L. setiferus (7.8‰) (Rosas et al.,
1999b), suggesting that F. brasiliensis is less resistant to salinity decreases than other
penaeid species.
The osmoregulatory capacity (OC) is a useful test to evaluate the physiological
conditions of shrimp in cultivation and to detect the effects of sublethal stress
(Charmantier et al., 1994). The OC has been related to temperature and developmental
stages of shrimp (Charmantier-Daures et al., 1988), to the molting stage, and to
variations in dissolved oxygen (Charmantier et al., 1994). According to these authors, a
higher OC means a greater capacity to compensate for a salinity change, which may be
reduced when the animals are in an adverse situation. The differences observed between
OC obtained from literature and that obtained from F. brasiliensis experiments could
indicate that F. brasiliensis and M. japonicus had a lower capacity to tolerate a diluted
environment than observed in other species (Fig. 2).
The slope of the relation between medium and hemolymph osmotic pressure has been
used to compare the OC among penaeid species (Castille and Lawrence, 1981; ParadoEstepa et al., 1987; Chen et al., 1992). When the slopes of this relation for different
penaeid shrimp are compared (Table 3), shrimp of the genus Litopenaeus and
Fenneropenaeus have the lowest values and those belonging to the genus Farfantepenaeus have the highest slope values. As the deviation of the isosmotic line reflects
the degree of regulation (slope 5 0 means osmoregulator, slope 5 1 means osmoconformer), organisms with high slope values have a poorer hyperosmotic regulation than
those that have low values of the slope (Castille and Lawrence, 1981).
Analyzing the differences in the OC, we can separate the shrimp that inhabit more
marine environments with greater hyporegulatory capacity (F. brasiliensis, M. japonicus,
F. aztecus, F. duorarum) from those that inhabit more estuarine environments with
greater hyperregulatory capacity (L. stylirrostris and L. setiferus) (Fig. 2, Table 3). The
260
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
Table 3
Slopes of the linear relation between hemolymph and medium osmotic pressure in different penaeid species
Species
Slope
Author
Litopenaeus stylirrostris
Fenneropenaeus chinensis
Litopenaeus stylirrostris
Litopenaeus vannamei
Litopenaeus setiferus
Litopenaeus setiferus
Fenneropenaeus indicus
Farfantepenaeus brasiliensis
Farfantepenaeus aztecus
Farfantepenaeus duorarum
0.16
0.189
0.20
0.20
0.20
0.23
0.24
0.33
0.38
0.40
Castille and Lawrence (1981)
Chen et al. (1992)
Charmantier and Aquacop (pers. comm.)
Castille and Lawrence (1981)
Rosas et al. (1999a)
Castille and Lawrence (1981)
Parado-Estepa et al. (1987)
This paper
Castille and Lawrence (1981)
Castille and Lawrence (1981)
OC of penaeid shrimp can be related to their distribution according to salinity. (Scelzo
´˜
and Zuniga,
1987) found juvenile F. brasiliensis in high densities in water slightly
hypersaline in the shallow Laguna La Restinga in Venezuela. Wenner and Beatty (1993)
found in estuarine habitats in South Carolina that the distribution peaks of L. setiferus
postlarvae coincide with a decrease in salinity in the area. In addition, the decrease in
salinity contributes to the movement of F. duorarum out of the area and the decrease in
salinity and temperature explain the low recruitment of this species into the estuarine
system. Zein-Eldin and Renaud (1986), who analyzed the influence of environmental
factors on the populations of F. aztecus and L. setiferus along the coast of Texas, have
reported similar behaviors. Though both species are found distributed in a wide range of
salinities, L. setiferus prefers lower salinities and stays near the coast to grow and
reproduce, whereas F. aztecus prefers higher salinities, increases their burying activity in
low salinities, and migrate to reproduce far away from the coast.
The isosmotic point of early juvenile F. brasiliensis (25‰, 794 mOsm kg 21 ) obtained
in the present study is within the range of isosmotic point found for many penaeid
species. For M. japonicus the isosmotic point is about 820 mOsm kg 21 in postlarvae and
880 mOsm kg 21 in adults, in F. chinensis, this point has been reported as 700 mOsm
kg 21 for postlarvae and 780 mOsm kg 21 for adults (Charmantier-Daures et al., 1988). In
F. indicus of 5–10 g, the isosmotic point was 780 mOsm kg 21 (24‰) (Parado-Estepa et
al., 1987). Castille and Lawrence (1981) reported the isosmotic point in F. aztecus
juveniles at 25.6‰, in F. duorarum at 26.3‰, in L. setiferus at 23.3‰, in L. stylirrotris
at 24‰, and in L. vannamei at 24.7‰. In Penaeus monodon, the isosmotic point is at
26‰ (Ferraris et al., 1986).
The isosmotic point has been associated with optimum conditions for growth of
penaeid shrimp. However, when comparing different isosmotic points reported and
optimum salinity for growth in different shrimp species, it is possible to observe that not
always does better growth coincide with the isosmotic point reported (Fig. 3). Some
species grow better in salinities above their isosmotic point (F. brasiliensis, this work;
M. japonicus, Liao, 1969, and P. esculentus, O’Brien, 1994), some have better growth in
salinities near the isosmotic point (F. indicus, P. monodon, and P. semisulcatus, Raj and
Raj, 1982), and a third group grow better in salinities below the isosmotic point (F.
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
261
Fig. 3. Optimum growth salinities (bars) and isosmotic point (♦) reported for several shrimp species. F.
brasiliensis (this paper), M. japonicus (Liao, 1969), P. monodon, F. indicus, P. semisulcatus (Raj and Raj,
1982), F. chinensis (Chen et al., 1992), F. aztecus (Venkataramiah et al., 1974), L. setiferus (Rosas et al.,
1999a), L. vannamei (Bray et al., 1994), P. esculentus (O’Brien, 1994).
aztecus, Venkataramiah et al., 1974; L. setiferus, Rosas et al., 1999b, and L. vannamei,
Bray et al., 1994). The different optimum salinities for growth in different species
generally correspond to the differences in their osmotic capacities. Species with higher
hyper-OC grow better in the lower salinities, whereas species with lower hyper-OC grow
better in the highest salinities. However this is not true for all penaeid species. F. aztecus
exhibits one of the highest values of the slope of the relation between the medium and
hemolymph osmotic pressure (Table 3), has a limited regulatory capacity, and has better
growth in relatively low salinities (8.5–17‰; Venkataramiah et al., 1974). Similarly,
Chen et al. (1992) found the best growth of F. chinensis in salinities around the
isosmotic point of 490 mOsm kg 21 (16.5‰), which is very different from the isosmotic
point reported by Charmantier-Daures et al. (1988) from 700 to 780 mOsm kg 21
(23–24‰) for the same species. Differences between these authors could be related to
the different molting stages that influence the osmotic pressure of the organisms
(Charmantier et al., 1994).
The results obtained in our work provide evidence that F. brasiliensis is a species
with limited capacity to tolerate low salinities and grows well in salinities greater than
its isosmotic point. Results show that the isosmotic point is not strongly related to
greater growth in this and some other penaeid shrimp. However, the osmotic capacity
seems to have a direct relation with the biological characteristics of the species that
determine environmental preferences and behavior, which in turn influence distribution
262
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
in the estuarine ecosystem. The possibility of correlating more biological aspects of
penaeid shrimp through evaluations of OC causes us to recommend the OC as the most
adequate way of presenting osmotic pressure results in penaeid species.
Acknowledgements
The present study was done through a collaboration agreement between Faculty of
Science of UNAM and Small Founding Program to Development – UNO. We express
our gratitude to the MUTIS foundation for the scholarship awarded to Roberto Brito.
´ de Atencion
´ al Personal Academico
´
This project was partially financed by Direccion
of
the UNAM (project No. 214596) and CONACyT (project No. 3293P-9607). [SS]
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244 (2000) 253–263
L
www.elsevier.nl / locate / jembe
Effect of salinity in survival, growth, and osmotic capacity
of early juveniles of Farfantepenaeus brasiliensis (decapoda:
penaeidae)
´
Roberto Brito a , Marıa-Eugenia
Chimal b , *, Carlos Rosas b
b
a
Center of Marine Research, Havana University, Havana, Cuba
Group of Experimental Marine Biology, Laboratory of Ecophysiology, Faculty of Sciences,
UNAM. Apdo. Post. 69, Ciudad del Carmen, Campeche, Mexico
Received 15 May 1999; received in revised form 26 June 1999; accepted 22 September 1999
Abstract
The effect of salinity in survival, growth and osmotic capacity of juvenile Farfantepenaeus
brasiliensis was determined. Survival was not affected by salinities from 15 to 35‰ during 96 h
exposure periods. Shrimps exposed to 5 and 10‰ were noticeably affected by salinity with a
survival of 0 and 48% after 96 h, respectively. Lethal salinity for 50% of the individuals in 96 h
(LS 50 , 96 h) at 288C was 10‰. Growth rate (mg dw day 21 ) was significantly higher at higher
salinities. The isosmotic point of early juvenile F. brasiliensis was 794 mOSm kg 21 , at around
25‰. Results indicate that F. brasiliensis has low tolerance to low saline environments, and grows
better in salinities greater than its isosmotic point. Osmotic capacity seemed to be related to
biological characteristics that determine the environmental preferences and behavior, as well as the
distribution of this shrimp species. 2000 Elsevier Science B.V. All rights reserved.
1. Introduction
Increased interest in the physiology of penaeid shrimp has derived from
the aquaculture industry in many regions of the world. Many studies have focused on
he biological aspects of several shrimp species, and increasing knowledge in this
research field has allowed optimal conditions for their culture. For Farfantepenaeus
brasiliensis, not much information of the biology is known, although it is distrib-
*Corresponding author.
0022-0981 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved.
PII: S0022-0981( 99 )00142-2
254
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
uted along the Florida coast in USA to the Bermudas and the Antilles, and along
the Atlantic coast of South America to Rio Grande do Norte, Brazil (Sandoval,
1996).
In Mexico, F. brasiliensis has great economic importance in the fishery around the
Peninsula of Yucatan. In this region, red shrimp are caught all year, mainly in the
´ ´
northwest of the Isla Contoy (Arreguın-Sanchez,
1981) and in a lesser amount in the
Gulf of Mexico toward Cabo Catoche (Silva Neto et al., 1982).
Little is known about this species, the present information is mainly on its distribution
and fishery. Biological and physiological aspects are virtually unknown; hence the need
to do research that contributes to the knowledge of the environmental requirements of F.
brasiliensis and to help establish a basis for its culture. To date, there are no studies that
approach, in any integral way, the effects of salinity on the physiology of this shrimp
species.
Postlarvae and juveniles are exposed to salinity, temperature, dissolved oxygen, and
pH changes characteristic of coastal environments. Numerous investigations have
demonstrated that when juveniles are exposed to environmental changes, there are
modifications in the ionic and osmotic balance (Dall and Smith, 1981; Castille and
Lawrence, 1981; Rosas et al., 1999a), respiratory activity (Dalla Via, 1986; Kutty et al.,
1971; Rosas et al., 1999a; Chen and Nan, 1995), assimilation and growth (Chen et al.,
1992; Ogle et al., 1992; Bray et al., 1994; Rosas et al., 1999b), and ammonia excretion
(Spaargaren et al., 1982; Chen and Lai, 1993; Chen and Nan, 1995). These results have
provided evidence that penaeid shrimp are well adapted to tolerate environmental
fluctuations.
According to Castille and Lawrence (1981), and Claybrook (1983), the adaptive
capacity of penaeid shrimps is specific and is determined by a number of evolutionary
factors that have caused shrimp species to be distributed differently in the estuarinemarine gradient. F. brasiliensis have been associated with a high saline environment
´˜
from north of Brazil to the Caribbean Sea (Scelzo and Zuniga,
1987; Sandoval, 1996).
For that reason, F. brasiliensis may be identified as have been F. aztecus and F.
duorarum as limited euryhaline shrimp species (Zein-Eldin and Renaud, 1986; Wenner
and Beatty, 1993). In that sense, (Venkataramiah et al., 1974) showed that such
characteristic could be related with limitation on physiological mechanisms associated
with the osmotic balance, which affect the energetic metabolism, the osmotic pressure,
and finally the growth. On this base is possible to think that limited capacity for osmotic
regulation of F. brasiliensis could be associated with the natural range distribution of
this species.
Osmotic capacity (OC) is a useful indicator to measure the stress of shrimp exposed
to a diversity of environmental factors, among them dissolved oxygen (Charmantier et
al., 1994; Rosas et al., 1999a) and pollutants (Lignot et al., 1997). Unpublished data
from studies in our laboratory have demonstrated that coupled to nitrogen excretion,
hemolymph glucose, and hepatopancreas glycogen levels, OC allow us to determine
optimum conditions for growth when shrimp are fed diets with different carbohydrate
levels. The objective of this study was to determine the effect of salinity on growth,
survival, and osmotic capacity of juvenile F. brasiliensis.
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
255
2. Material and methods
2.1. Origin of the animals
The postlarvae and early juveniles of Farfantepeneus brasiliensis used in the
experiments were bred in the Group of Experimental Marine Biology, Faculty of
Sciences, UNAM, in Ciudad del Carmen, Campeche, from spawners captured along the
coasts of Quintana Roo, Mexico. Larvae from naupli I to postlarva 27 (PL 27 , 27 days
after the last metamorphic molt) were maintained in a fiberglass tank of 400 l capacity,
at 37‰ salinity, constant aeration, and pH . 8. Larvae were fed a mixture of unicellular
algae (diatoms and flagellates) and freshly hatched artemia nauplii to PL 5 (Gallardo et
al., 1995). At PL 6 , shrimp were fed a mixture of artemia nauplii (25%) and balanced
food (75%) with 50% protein at 120% of body weight.
2.2. Tolerance to abrupt salinity changes
To determine survival rate, shrimp at PL 28 were transferred without previous
acclimatization from rearing salinity (37‰) to water at 5, 10, 15, 20, 25, 30, and 35‰.
Ten postlarvae in each salinity treatment (three replicates per treatment) were placed in
5 l plastic containers, and the postlarvae surviving after 96 h counted.
Water in each treatment was prepared the day before the experiments by diluting
filtered (5 mm) and ultraviolet sterilized seawater with commercial purified water. The
salinity was determined using an Atago refractometer with 61‰ precision. Organisms
were maintained under controlled experimental conditions of temperature (288C),
photoperiod (12 h:12 h, light: dark) with lighting between 280 and 650 lux, and constant
aeration. Shrimp were fed pellet food G-GAX (Gaxiola, 1994) with 50% protein and
with particle size between 210 and 300 mm at 20% of body weight, and with freshly
hatched artemia nauplii. Shrimp were fed two times daily at 1000 and 1800 throughout
the experiments. Daily water exchange was 50% in all the experimental tanks, with
feces, sheds, and remaining food being withdrawn from all containers. The absence of
movement and absence of response to touch were the criteria for death. Surviving
shrimp were counted at 0.5, 1, 2, 4, 6, 8, 12, 24, 36, 48, 72, and 96 h of exposure in each
treatment. Dead shrimp were removed at time of each observation.
2.3. Osmotic pressure
Early juvenile F. brasiliensis (248616 mg ww) were transferred directly from 37‰ to
salinities of 5, 10, 15, 20, 25, 30, 35, and 40‰ at a temperature of 288C. After 2 h in
these conditions, shrimp were dried on absorbent paper and samples of hemolymph (20
ml from one to three individuals) were taken using a hypodermic needle inserted in the
heart (n between 7 and 17 samples). Osmotic pressure of three water samples in each
treatment was also measured. To measure the osmotic pressure, a microosmometer (3
MO Plus, Advanced Instruments, Inc., Norwood, Massachusetts, USA) was used. Only
shrimp in the intermolt stage were used for these determinations.
256
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
2.4. Growth and survival in different salinities
Before the experiments, a group of 40 individuals was randomly selected, dried on
absorbent paper, and weighed on an OHAUS analytical balance (60.0001 g) to obtain
their initial wet weight. Thereafter, individuals were dried in a stove at 608C for 24 h
and were weighed to obtain the dry weight.
The effect of the salinity on growth and survival of shrimp was studied in animals
acclimated to three salinities; 15, 25 and 35‰. Sixteen PL 34 were placed in 30L plastic
tanks, which were used in each treatment (one replicate per treatment). Shrimp used in
15 and 25‰ salinities were acclimated through a device that supplies tap water to the
experimental tanks until the required salinity was obtained (48 h). However, those
treated at 35‰ were transferred directly from seawater of 37‰.
Shrimp were maintained for 60 days at constant temperature (288C), with a
photoperiod of 12 h: 12 h, light: dark, and constant aeration. Shrimp were fed two times
a day (pellets G-GAX, 50% protein) at 20% of body weight. Daily water exchange was
50% in all the experimental tanks. Feces, sheds, and the remaining food were eliminated
every day during water exchange. Surviving shrimp were counted and temperature, pH,
and dissolved oxygen were recorded on a daily basis. At the end of the experiment,
shrimp were dried and weighed as described previously.
Differences in osmotic pressure, final weight, and growth rate between treatments
were analyzed by one-way analysis of variance. When significant differences were
found, Duncan’s Multiple Range test was used to identify significant differences
between treatments. Differences are reported as statistically significant when P , 0.05
(Zar, 1984). The program STATISTICA 4.5 was used for statistic analysis.
3. Results
3.1. Tolerance to abrupt salinity changes
Survival of postlarval F. brasiliensis was not affected by salinities between 15 and
35‰ during 96 h exposure (Fig. 1). By contrast, shrimps at 10 and 5‰ were affected by
salinity with survival of 48 and 0%, respectively, after 96 h. Lethal salinity LS 50 for 96
h was 10‰ (Fig. 1).
3.2. Osmotic pressure ( OP)
The isosmotic point of early juvenile F. brasiliensis (248616 mg ww) was found
around 25‰ (794 mOsm kg 21 ), a salinity under which the animals were hyperosmotic.
The highest OP was recorded in shrimp at 35‰ (872 mOsm kg 21 ), and it was
significantly different from the OP in 25‰, 40‰, 15–20–30‰, 10‰ and 5‰ salinities
(P , 0.05). The OP of shrimp at 35‰ was 2.3 times that at 5‰ (Table 1) (P , 0.05).
There was found a significant linear relation between medium and hemolymph osmotic
pressure with a slope value of 0.33 (r 2 5 0.68, F 5 12.80, P 5 0.01).
The osmoregulatory capacity (OC) of early juvenile F. brasiliensis varied with
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
Fig. 1. F. brasiliensis (PL
28
257
) survival in different salinities.
salinity. The hypo-OC of shrimp at 40‰ (2421 mOsm kg 21 ) was 2.3 times greater than
that in animals at 30 and 35‰ (average of 2 180 mOsm kg 21 ) (P , 0.05). The lowest
hyper-OC was observed in shrimp at 25‰ (40 mOsm kg 21 ), and increased with
decreasing salinity until it reached its maximum value in shrimp at 10‰ (287 mOsm
kg 21 ). The hyper-OC of animals at 5‰ (251 mOsm kg 21 ) was similar to that in shrimp
at 15‰ (246 mOsm kg 21 ). Fig. 2 shown the OC for several penaeid species, comparing
the OC in extreme salinities, we can separate F. brasiliensis with the highest hypo-OC
from F. chinensis and L. stilyrrostris, when analyzing the hyper-OC, F. brasiliensis and
M. japonicus have the lowest values and L. stylirrostris and L. setiferus the highest
values.
3.3. Growth and survival in different salinity treatments
During growth experiments, water temperature was maintained at 2860.58C, pH
Table 1
F. brasiliensis juveniles and culture water osmotic pressure (mOsm kg 21 ) in different salinities a
Salinity
(‰)
5
10
15
20
25
30
35
40
Shrimp
n
Mean
S.E.
14
380 ( f )
13.9
14
603 (e)
8.1
10
733 (d )
11.5
14
714 (d )
4.9
7
833 ( b)
9.1
11
737 (d )
11.0
17
872 (a)
10.1
13
798 (c)
13.8
Water
n
Mean
S.E.
3
186
1.4
3
307
0.6
3
487
0.5
3
598
3.0
3
794
1.4
3
905
1.2
3
1071
2.8
3
1219
1.2
a
Different letters mean statistical differences (P , 0.05).
F ( p)
179.4
( , 0.001)
258
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
Fig. 2. Osmoregulatory capacity of several shrimp species exposed to salinity changes. F. chinensis (–h–,
Charmantier-Daures et al., 1988), L. vannamei (–m–, Charmantier et al., 1994), L. stylirostris (–♦–,
Charmantier and Aquacop, pers. comm.), M. japonicus (– 3 –, Charmantier et al., 1988), L. setiferus (–j–,
Rosas et al., 1999a), F. brasiliensis (–d–, this paper).
varied between 8.00260.106 in 15‰ and 8.17860.100 in 35‰. Dissolved oxygen was
kept close to the saturation level, varying from 6.9560.20 in 15‰ to 6.2860.15 mgO 2
l 21 in 35‰ salinity. Final body weights and growth rates (mg dw day 21 ) were
significantly greater in shrimp maintained at 35‰ (P , 0.05) (Table 2). Tissue water
content was not affected by the different treatments. For 62 to 64 days, salinity did not
affect the survival of shrimp maintained in any of the three experimental salinities
(93.8% survival) (Table 2).
Table 2
Growth rate (mg day 21 ), body water (%), and survival (%) of F. brasiliensis in different salinities.
Mean6S.E.a
SALINITY ‰
Initial wet weight, mg
Initial dry weight, mg
n
Final wet weight, mg
Final dry weight, mg
n
Days of culture
Growth rate, mg dw day 21
Body water, %
Survival, %
a
15
25
35
21061.1
4.7960.2
41
500621 b
12765 b
12
62
1.9860.09 b
74.560.4
93.8
21061.1
4.7960.2
41
462632 b
122611 b
7
63
1.8760.18 b
73.760.9
93.8
21061.1
4.7960.2
41
568623 a
15166 a
11
64
2.3060.09 a
73.260.06
93.8
Different letters mean statistical differences (P , 0.05).
F (P)
4.25 (0.02)
4.46 (0.02)
3.61 (0.04)
1.27 (0.29)
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
259
4. Discussion
Postlarval (PL 28 ) F. brasiliensis showed a wide range of tolerance to salinity changes,
which closely corresponds with the adaptive mechanisms in penaeids that, at this stage
of their life cycle, inhabit estuarine zones and are exposed to variable salinity. Postlarval
F. brasiliensis grow in coastal lagoons or estuaries for 2 to 4 months before they migrate
into the marine environment for reproduction (Sandoval, 1996).
Lethal salinity for 50% of the animals (LS 50 ) varies among species and depends on
the temperature and developmental stages of the organisms under study. CharmantierDaures et al. (1988) found that in Marsupenaeus japonicus PL 20 – 60 the SL 50 decreased
with increasing temperature, whereas in Fenneropenaeus chinensis, a relation between
SL 50 and temperature did not appear to be so direct, and PL 60 was more resistant to
salinity changes than PL 20 . L. vannamei increases its resistance to salinity changes as
increasing postlarval development (Aquacop et al., 1991; Ogle et al., 1992; Samocha et
al., 1998). In M. japonicus, the 24 h LS 50 at 258C decreased from larval stages to PL 10
stage (Charmantier et al., 1988), corresponding to migrations from the marine ambient
to the estuarine nursery areas that occur during these stages. LS 50 at 288C in PL 28 F.
brasiliensis obtained in the present study was found at 10‰, which was similar to those
reported for PL 40 – 60 for F. chinensis at 258C (10.2–10.5‰) (Charmantier-Daures et al.,
1988) and greater than that found for PL 10 – 21 stages of L. setiferus (7.8‰) (Rosas et al.,
1999b), suggesting that F. brasiliensis is less resistant to salinity decreases than other
penaeid species.
The osmoregulatory capacity (OC) is a useful test to evaluate the physiological
conditions of shrimp in cultivation and to detect the effects of sublethal stress
(Charmantier et al., 1994). The OC has been related to temperature and developmental
stages of shrimp (Charmantier-Daures et al., 1988), to the molting stage, and to
variations in dissolved oxygen (Charmantier et al., 1994). According to these authors, a
higher OC means a greater capacity to compensate for a salinity change, which may be
reduced when the animals are in an adverse situation. The differences observed between
OC obtained from literature and that obtained from F. brasiliensis experiments could
indicate that F. brasiliensis and M. japonicus had a lower capacity to tolerate a diluted
environment than observed in other species (Fig. 2).
The slope of the relation between medium and hemolymph osmotic pressure has been
used to compare the OC among penaeid species (Castille and Lawrence, 1981; ParadoEstepa et al., 1987; Chen et al., 1992). When the slopes of this relation for different
penaeid shrimp are compared (Table 3), shrimp of the genus Litopenaeus and
Fenneropenaeus have the lowest values and those belonging to the genus Farfantepenaeus have the highest slope values. As the deviation of the isosmotic line reflects
the degree of regulation (slope 5 0 means osmoregulator, slope 5 1 means osmoconformer), organisms with high slope values have a poorer hyperosmotic regulation than
those that have low values of the slope (Castille and Lawrence, 1981).
Analyzing the differences in the OC, we can separate the shrimp that inhabit more
marine environments with greater hyporegulatory capacity (F. brasiliensis, M. japonicus,
F. aztecus, F. duorarum) from those that inhabit more estuarine environments with
greater hyperregulatory capacity (L. stylirrostris and L. setiferus) (Fig. 2, Table 3). The
260
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
Table 3
Slopes of the linear relation between hemolymph and medium osmotic pressure in different penaeid species
Species
Slope
Author
Litopenaeus stylirrostris
Fenneropenaeus chinensis
Litopenaeus stylirrostris
Litopenaeus vannamei
Litopenaeus setiferus
Litopenaeus setiferus
Fenneropenaeus indicus
Farfantepenaeus brasiliensis
Farfantepenaeus aztecus
Farfantepenaeus duorarum
0.16
0.189
0.20
0.20
0.20
0.23
0.24
0.33
0.38
0.40
Castille and Lawrence (1981)
Chen et al. (1992)
Charmantier and Aquacop (pers. comm.)
Castille and Lawrence (1981)
Rosas et al. (1999a)
Castille and Lawrence (1981)
Parado-Estepa et al. (1987)
This paper
Castille and Lawrence (1981)
Castille and Lawrence (1981)
OC of penaeid shrimp can be related to their distribution according to salinity. (Scelzo
´˜
and Zuniga,
1987) found juvenile F. brasiliensis in high densities in water slightly
hypersaline in the shallow Laguna La Restinga in Venezuela. Wenner and Beatty (1993)
found in estuarine habitats in South Carolina that the distribution peaks of L. setiferus
postlarvae coincide with a decrease in salinity in the area. In addition, the decrease in
salinity contributes to the movement of F. duorarum out of the area and the decrease in
salinity and temperature explain the low recruitment of this species into the estuarine
system. Zein-Eldin and Renaud (1986), who analyzed the influence of environmental
factors on the populations of F. aztecus and L. setiferus along the coast of Texas, have
reported similar behaviors. Though both species are found distributed in a wide range of
salinities, L. setiferus prefers lower salinities and stays near the coast to grow and
reproduce, whereas F. aztecus prefers higher salinities, increases their burying activity in
low salinities, and migrate to reproduce far away from the coast.
The isosmotic point of early juvenile F. brasiliensis (25‰, 794 mOsm kg 21 ) obtained
in the present study is within the range of isosmotic point found for many penaeid
species. For M. japonicus the isosmotic point is about 820 mOsm kg 21 in postlarvae and
880 mOsm kg 21 in adults, in F. chinensis, this point has been reported as 700 mOsm
kg 21 for postlarvae and 780 mOsm kg 21 for adults (Charmantier-Daures et al., 1988). In
F. indicus of 5–10 g, the isosmotic point was 780 mOsm kg 21 (24‰) (Parado-Estepa et
al., 1987). Castille and Lawrence (1981) reported the isosmotic point in F. aztecus
juveniles at 25.6‰, in F. duorarum at 26.3‰, in L. setiferus at 23.3‰, in L. stylirrotris
at 24‰, and in L. vannamei at 24.7‰. In Penaeus monodon, the isosmotic point is at
26‰ (Ferraris et al., 1986).
The isosmotic point has been associated with optimum conditions for growth of
penaeid shrimp. However, when comparing different isosmotic points reported and
optimum salinity for growth in different shrimp species, it is possible to observe that not
always does better growth coincide with the isosmotic point reported (Fig. 3). Some
species grow better in salinities above their isosmotic point (F. brasiliensis, this work;
M. japonicus, Liao, 1969, and P. esculentus, O’Brien, 1994), some have better growth in
salinities near the isosmotic point (F. indicus, P. monodon, and P. semisulcatus, Raj and
Raj, 1982), and a third group grow better in salinities below the isosmotic point (F.
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
261
Fig. 3. Optimum growth salinities (bars) and isosmotic point (♦) reported for several shrimp species. F.
brasiliensis (this paper), M. japonicus (Liao, 1969), P. monodon, F. indicus, P. semisulcatus (Raj and Raj,
1982), F. chinensis (Chen et al., 1992), F. aztecus (Venkataramiah et al., 1974), L. setiferus (Rosas et al.,
1999a), L. vannamei (Bray et al., 1994), P. esculentus (O’Brien, 1994).
aztecus, Venkataramiah et al., 1974; L. setiferus, Rosas et al., 1999b, and L. vannamei,
Bray et al., 1994). The different optimum salinities for growth in different species
generally correspond to the differences in their osmotic capacities. Species with higher
hyper-OC grow better in the lower salinities, whereas species with lower hyper-OC grow
better in the highest salinities. However this is not true for all penaeid species. F. aztecus
exhibits one of the highest values of the slope of the relation between the medium and
hemolymph osmotic pressure (Table 3), has a limited regulatory capacity, and has better
growth in relatively low salinities (8.5–17‰; Venkataramiah et al., 1974). Similarly,
Chen et al. (1992) found the best growth of F. chinensis in salinities around the
isosmotic point of 490 mOsm kg 21 (16.5‰), which is very different from the isosmotic
point reported by Charmantier-Daures et al. (1988) from 700 to 780 mOsm kg 21
(23–24‰) for the same species. Differences between these authors could be related to
the different molting stages that influence the osmotic pressure of the organisms
(Charmantier et al., 1994).
The results obtained in our work provide evidence that F. brasiliensis is a species
with limited capacity to tolerate low salinities and grows well in salinities greater than
its isosmotic point. Results show that the isosmotic point is not strongly related to
greater growth in this and some other penaeid shrimp. However, the osmotic capacity
seems to have a direct relation with the biological characteristics of the species that
determine environmental preferences and behavior, which in turn influence distribution
262
R. Brito et al. / J. Exp. Mar. Biol. Ecol. 244 (2000) 253 – 263
in the estuarine ecosystem. The possibility of correlating more biological aspects of
penaeid shrimp through evaluations of OC causes us to recommend the OC as the most
adequate way of presenting osmotic pressure results in penaeid species.
Acknowledgements
The present study was done through a collaboration agreement between Faculty of
Science of UNAM and Small Founding Program to Development – UNO. We express
our gratitude to the MUTIS foundation for the scholarship awarded to Roberto Brito.
´ de Atencion
´ al Personal Academico
´
This project was partially financed by Direccion
of
the UNAM (project No. 214596) and CONACyT (project No. 3293P-9607). [SS]
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