Aquaculture 244 (2005) 341 – 348
www.elsevier.com/locate/aqua-online
The combined effects of salinity and temperature
on the oxygen consumption of juvenile shrimps
Litopenaeus stylirostris (Stimpson, 1874)
Milton Spanopoulos-Hernándeza, Carlos A. Martı́nez-Palaciosb,*,
Ruth C. Vanegas-Pérezc, Carlos Rosasd, Lindsay G. Rosse
a
b
Laboratorio de Hidrologı́a, Instituto Tecnológico del Mar, Mazatlán, P. O. Box 757 C. P. 82000 Mazatlán Sinaloa, Mexico
Universidad Michoacana de San Nicolás de Hidalgo. Av. San Juanito Itzicuaro s/n C.P. 58330 Morelia Michoacán, Mexico
c
Laboratorio de Ecofisiologı́a, Fac. de Ciencias, UNAM, México 04510, D.F., Mexico
d
Laboratorio de Ecologı́a y Biologı́a Marina Experimental, Fac. de Ciencias UNAM. Calle 8A,
No. 248 x 5 Vista Alegre Norte, Mérida 97130, Yucatán, México
e
Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA Scotland, UK
Received 31 March 2004; received in revised form 23 November 2004; accepted 23 November 2004
Abstract
The respiratory rates of Litopenaeus stylirostris were measured at three different salinities (20, 30, and 40) and temperatures
(20, 30, and 35 8C). Equations of routine oxygen consumption (VO2) and weight-specific oxygen consumption (QO2) were
obtained for the nine combinations and regression models for the effects of temperatures and salinities were derived from the data.
Temperature, salinity, and combinations of salinity and temperature had a significant effect on oxygen consumption rate ( pN0.05).
The lowest values were found at a salinity of 30, suggesting that the iso-osmotic point may be at about this value. The thermal
coefficient (Q10) did not vary with salinity, but did vary with temperature. Q10 was 0.62 between 20 and 30 8C, 2.5 between 30 and
35 8C, and 1.88 over the full temperature range. The partial coefficients and the multiple regression equation were highly
significant suggesting that culture of this species would be optimum at salinities between 25–38 and temperatures of 20–30 8C.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Shrimp; Litopenaeus stylirostris; Respiration; Salinity; Temperature; Q10
1. Introduction
* Corresponding author. Tel.: +52 4433272350; fax: +52
4433272350.
E-mail address: [email protected] (C.A. Martı́nez-Palacios).
0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2004.11.023
Among the diverse problems faced by aquaculture,
oxygen availability for organisms under culture is a
critical feature. Oxygen is essential for intermediate
metabolism where it participates in different oxidative
342
M. Spanopoulos-Hernández et al. / Aquaculture 244 (2005) 341–348
activities releasing the energy necessary for biological
work (Prosser and Brown, 1968). Oxygen requirements and oxygen consumption rates vary considerably depending upon a wide range of biotic and
abiotic factors including activity, environmental temperature, salinity, body weight, and diet (Brett, 1987).
Low oxygen concentrations can result in variations in
the energetic systems of organisms and can affect
feeding, growth, and reproduction (Martı́nez-Palacios
and Ross, 1994).
The most important abiotic factors affecting oxygen consumption in aquatic organisms are temperature and salinity (Brett, 1987). Temperature directly
affects the rate of all biological processes and salinity
places an osmoregulatory demand on organisms. Both
have effects on the oxygen content of the medium. In
addition to the effects of the individual variables, the
interaction of salinity and temperature can be complex, with one variable acting as a modulating factor
on the effects of the other (Vernberg, 1983).
The temperature coefficient (Q10) represents the
degree of sensitivity of an organism to temperature
(Dı́az-Iglesia, 1988) and an evaluation of oxygen
consumption at different temperatures allows the
calculation of the thermal coefficient of poikilotherm
organisms from aquatic habitats (Ross and Ross, 1983;
Kurmaly et al., 1989; Villareal and Ocampo, 1993;
Villareal and Rivera, 1993; Carvalho and Phan, 1997).
In the culture of penaeid shrimps, oxygen consumption
under different conditions of salinity and temperature is
indicative of the consumed energy (Rosas et al., 1996).
This information is useful for estimating the initial
requirements of water flow as a function of the density
of organisms in ponds or other culture facilities.
Several authors have examined the effect of salinity
and temperature on oxygen consumption in shrimp
(Seidman and Lawrence, 1985; Martı́nez-Palacios and
Ross, 1994; Rosas et al., 1997). The effect of temperature and salinity on a given species is not the same for
all life stages, physiological variations are age-dependent so metabolic responses can vary (Vernberg, 1983).
Gaudy and Sloane (1981) reported a slight increase of
the metabolism of L. stylirostris post larvae, at low
salinities.
This work investigates the effects of temperature,
salinity, and the interaction of these variables on the
resting respiratory rate of juvenile blue shrimps L.
stylirostris.
2. Materials and methods
2.1. Animals
Shrimp in the weight range 4 to 14 g were obtained
from a commercial hatchery in Sinaloa, Mexico, and
held in tanks of 600 L capacity at a salinity of 35 and
25 8C with aeration and 10% per day water replacement. Dissolved oxygen, temperature, and salinity
were monitored using an oxygen meter (YSI Model
59, Yellow Springs Instrument Company OH, USA),
a portable refractometer (ATAGO), and a mercury
thermometer. Animals were fed ad libitum twice a day
for a seven day period, using a commercial shrimp
diet containing 35% protein and 8% lipid.
2.2. Respirometers and experimental protocol
The respirometers were based upon the semiclosed flow design described by Ross and Ross
(1983). Glass chambers of 50 mL were used for
shrimps up to 5 g body weight, 250 mL for shrimp up
to 10 g body weight, and 500 mL for shrimp up to 15
g body weight. A 120 Am, mesh filter was placed over
the entrance of the respirometers to reduce the
introduction of particulate materials. Photoperiod
was 12L/12D and light intensity at the surface of
the respirometers was 400 lx (Lorenzo photometer,
model DL355ME216). Feeding of specimens ceased
24 h before measurements. Shrimps taken from stock
were weighed and then transferred to one of a set of
four respirometers initially under open flow conditions. On closure of the respirometer circuit, dissolved
oxygen (D.O.) in the circulating water was measured
using a YSI Model 59 oxygen meter. Measurements
were continued until a steady decline in D.O. was
recorded and did not extend beyond 15 min. This
procedure was then repeated with the other respirometers. A fifth, empty, respirometer was used
simultaneously in each trial as a control so that
background corrections could be made.
2.3. Oxygen consumption during acclimation of
juvenile L. stylirostris to the respirometers
Four unfed animals ranging from 9.2 to 13.1 g wet
weight were immersed in seawater (35 and 25 8C) in
complete darkness in the four respirometer chambers.
M. Spanopoulos-Hernández et al. / Aquaculture 244 (2005) 341–348
Table 1
Oxygen consumption in juveniles of L. stylirostris at 35 and 25 8C
after introduction to the respirometer
Shrimp
Oxygen consumption (mg/h/individual)
Hour 0
Hour 1
Hour 2
Hour 3
Hour 4
1
2.73
3.27
2.18
1.63
1.09
2
3.22
2.68
2.68
2.68
2.14
3
3.39
3.39
1.45
1.94
1.94
4
5.5
2.75
2.20
1.65
1.10
Mean
3.71a
3.02b
2.13c
1.97c
1.57c
Standard deviation F1.22 F0.36 F0.50 F0.49 F0.55
343
calculated using Statistica 5.5 and was tested by using
the coefficients obtained and an analysis of variance
( pb0.05).
Using data from 221 specimens from all treatments
ranging from 4.0 to 13.9 g, the thermal coefficient
(Q10) was calculated using the equation:
Q10 ¼ ðK2 =K1 Þ10=t2t1
ð1Þ
Where, K 1 and K 2 are the metabolic rates at temperatures t 1 and t 2, respectively (Dı́az-Iglesia, 1988).
Values with different superscripts are significantly different
( pb0.05).
3. Results
Oxygen consumption rates were measured immediately and each hour for 4 h following introduction to
the chambers. Differences in respiratory rate inside the
respirometer were tested for significance. Data were
tested for homoscedasticity and normality by a
Bartlett and Lilliefor test, and further comparisons
were made through an analysis of variance and a
Tukey test (Zar, 1984).
2.4. The effect of temperature and salinity on oxygen
consumption
Groups of shrimp were acclimated to the combinations of experimental temperature (20, 30, and 35
8C) and salinity (20, 30, and 40) for 48 h. Animals
were then introduced into the respirometers chambers
and, following acclimation periods of at least 4 h
derived from the previous experiment, resting oxygen
consumption was measured in unfed shrimp of 4.0 to
13.9 g wet body weight.
3.1. Oxygen consumption during acclimation of
juvenile L. stylirostris to the respirometers
Oxygen consumption per animal (VO2) during the
period inside respirometers decreased with time
(Table 1). The major reduction in respiration rate
was achieved about 2 h after handling and although
the rates were still reducing after 4 h, the mean
responses after 2, 3, and 4 h were not significantly
different ( pb0.05). In all further experiments, a
minimum period of 4 h was used before measurements were made.
3.2. The effect of temperature and salinity on oxygen
consumption
The effects of salinity and temperature on
weight-specific resting metabolism (QO2) in a 4 g
juvenile L. stylirostris are shown in Fig. 1. In
2.5. Statistical analysis
Regression equations for oxygen consumption per
animal (VO2) versus weight were obtained for every
combination of salinity and temperature. From these
data, the weight-specific oxygen consumption rate
(QO2) was calculated. Analysis of covariance (Zar,
1984) was used to define significant differences among
the combined effects of temperature and salinity on
oxygen consumption. Combinations which were different were identified using a Tukey test (Zar, 1984). A
multiple regression analysis of QO2 with respect to
salinity, temperature, and wet body weight was
Fig. 1. Weight-specific oxygen consumption (QO2 mg/kg/h) of
juvenile L. stylirostris of 4 g body weight at three salinities and
temperatures.
344
M. Spanopoulos-Hernández et al. / Aquaculture 244 (2005) 341–348
Table 2
Regression equations of oxygen consumption and weight-specific oxygen consumption in juveniles L. stylirostris for different salinities and
temperatures; W=wet body weight
Salinity
Temperature 8C
n
Individual oxygen
consumption VO2
(mgO2/h/animal)
Weight-specific
oxygen consumption
QO2 (mg/kg/h)
r
20
20
20
30
30
30
40
40
40
20
30
35
20
30
35
20
30
35
16
31
15
23
40
16
32
29
19
22.50W0.6028
130.85W0.8297
68.34W0.6351
46.24W0.7635
131.54W0.8824
84.81W0.7159
46.62W0.6911
185W0.8394
123.52W0.6806
22.49W0.3972
130.85W0.1703
68.34W0.3649
46.24W0.2365
131.54W0.1176
84.81W0.2841
46.61W0.3089
185W0.1606
123.52W0.3194
0.55
0.61
0.73
0.59
0.51
0.75
0.66
0.49
0.49
general, respiratory rate increased in direct proportion to temperature. Although the differences were
not significant ( pN0.05), oxygen consumption at all
experimental temperatures was lower at 30. The
equations of oxygen consumption per animal (VO2
mg/h) and weight-specific oxygen consumption
(QO2 mg/kg/h1) (Table 2) show a significant
correlation ( pb0.05) between routine metabolism
and wet weight of juvenile L. stylirostris exposed to
different salinity and temperature values. The bifactorial analysis of covariance shows that there is
an effect of temperature and salinity on the oxygen
consumption ( pb0.05) (Table 3). The combined
effect of salinity and temperature has a significant
( pb0.05) effect on the oxygen consumption of
juvenile L. stylirostris over the weight range
examined. Analysis of covariance (ANCOVA) and
multiple comparison test for each experimental
equation showed that there are significant differences between treatments ( pb0.05). It can be seen
that between 20 and 30 8C Q10 values were below 1
and between 30 and 35 8C Q10 was higher than 2
(Table 4). Over the full range, Q10 was just less
than 2.
The overall relationship between weight-specific
oxygen consumption of juvenile L. stylirostris and
Table 3
Analyses of VO2 responses to different temperatures and salinities by juvenile Litopenaeus stylirostris
(a) ANOVA of salinity, temperature, and their interactions
Source
Degrees of freedom
Sum of squares (SS)
MS
F calculated
F (0.5,2,211)
Significance p
Temperature
Salinity
Interaction
Error
2
2
4
211
11135.71
16356.35
56623.05
354981.62
5567.85
8178.17
14155.76
1682.38
3.3095
4.8611
8.4141
3.04
3.04
2.85
pb0.05
pN0.05
pb0.05
(b) ANCOVA and multiple comparisons for the regression equations of VO2 (from Table 2)
Slopes (b)
Ordinates to the origin (a)
F
b common
F
0.17 ( pN0.05)
0.74
27.00 ( pb0.05)
Multiple comparisons*
a
20–20 b20–30 b20–35
30–20 b30–30 b30–35
ab
40–20c40–30 c40–35
a
* Groups with different superscripts are significantly different ( Pb0.05).
M. Spanopoulos-Hernández et al. / Aquaculture 244 (2005) 341–348
Table 4
Thermal coefficient (Q10) in juveniles of L. stylirostris for different
temperature ranges and salinities
Salinity
Temperature intervals
20–30 8C
20–35 8C
30–35 8C
20
30
40
0.60
0.68
0.57
1.86
1.79
1.99
2.34
2.61
2.57
salinity, temperature, and wet body weight within the
experimental range can be summarised by the equation:
lnQO2 ¼ 3:6061 þ 0:01614S þ 0:06394T
32:23164W
ð2Þ
where lnQO2=natural logarithm of weight-specific
oxygen consumption rate, S=salinity () Y=temperature
(8C), and W=wet body weight. Analysis of variance
and partial coefficients (Table 5a) show that QO2 was
dependent on salinity, temperature, and body weight
with a high degree of significance. The regression
coefficients show that almost 84% of the data can be
explained by these relationships (Table 5b).
4. Discussion
It is important in respirometry to evaluate initial
stress and acclimation time for post-handling adaptation to the respirometers chambers. After 2 h, there
was no significant difference in the oxygen consumption rate (VO2) of juvenile L. stylirostris,
345
suggesting that after this time the shrimp had overcome the manipulation effects. In practice, about 4 h
is probably necessary. Kutty et al. (1971) reported that
a period of only 1 h was required for acclimation in
Penaeus indicus and Liao and Murai (1986) suggested that 2 h was required for P. monodon.
Martı́nez-Palacios et al. (1996) showed that Litopenaeus vannamei required 4 h.
The adaptation of an organism involves integrated
responses to the changes of environmental parameters
depending on species-specific homeostatic control
mechanisms. Such integrated responses may be
exerted at different biochemical, physiological, and
behavioural levels. The factorial plan of experiments
used in the present study allows detection of not only
the effects due to single variables, but also the effects
due to synergistic interaction between salinity and
temperature. Temperature was clearly the governing
factor on oxygen consumption of L. stylirostris
because shrimp had a higher resting metabolism at
35 8C than that observed at 30 or 20 8C. At the same
time an increment in oxygen consumption related to
an increment in salinity was observed indicating that
both environmental factors induced homeostatic metabolic adjustments.
The Q10 is a measure of the metabolic capacity of
aquatic animals to make adjustments after a temperature change. For metabolic rates of aquatic animals,
Q10 values are generally close to 2 indicating that the
metabolic rate increases twofold for a temperature
change of 10 8C. Q10 has been recognized as a
common value that reflects the adjustments related to
the enzymatic and physiological requirements for
Table 5
Analysis of QO2 responses to different temperatures and salinities by juvenile Litopenaeus stylirostris
(a) ANOVA of salinity temperature and body weight
Variables
Factors
Standard error
t (217)
p
Intercept
Salinity
Temperature
Body weight
3.6061
0.0161
0.0639
32.2316
0.08180
0.00184
0.00199
3.4530
44.08
11.12
31.96
9.33
b0.05
b0.05
b0.05
b0.05
(b) Analysis of multiple regression
R
R2
R 2 adjusted
Sum of squares
Degrees of freedom
MS
F
Significance p
0.9171
0.8412
0.8390
Model 33.56
Residual 6.33
Model 3
Residual 217
Model 11.1895
Residual 0.0292
38.25
b0.05
346
M. Spanopoulos-Hernández et al. / Aquaculture 244 (2005) 341–348
energy when temperature increases within the natural
range (Vernberg, 1983). In the present study, Q10
values obtained for L. stylirostris show that the
response to temperature for this species is around 2
when this index was calculated between 20 and 35 8C
and between 30 to 35 8C in shrimp exposed to all
experimental salinities. This indicates that this range
of temperature and salinity combinations reflects the
natural range of L. stylirostris because there were no
strong modifications in metabolism. Similar results
were obtained in P. monodon exposed to wide
temperature–salinity and dissolved oxygen ranges
(Salvato et al., 2001). Values of Q10 less than 2 in
the lower temperature range were observed indicating
that L. stylirostris has only partial compensation in the
range 20 to 30 8C (Prosser, 1990). In general, these
metabolic effects suggest that the adaptation limits of
this species are around 20 8C for all experimental
salinities. Similar results were observed by Villareal
and Rivera (1993) in Farfantopenaeus californiensis
at 19 8C.
At a salinity of 40 and 35 8C, oxygen consumption
in L. stylirostris was significantly different to all other
combinations. It is possible that this species has
problems to adapt at 35 8C because this temperature is
beyond the upper limit for the species (Mair, 1980).
Similarly, QO2 at 20 8C for juvenile L. stylirostris in
this work was comparable to values for F. californiensis (Villareal and Ocampo, 1993) at 19 8C in a
wet weight range from 2.3 to 10.0 g (181 mgO2/kg/
Table 6
Oxygen consumption Values (QO2) for some crustaceous of commercial importance
Species
Weight (g)
Salinity
Temperature (8C)
QO2 (mgO2/kg/h)
Author
P. japonicus
P. monodon
L. schmitti
L. schmitti
L. schmitti
F. californiensis
12.8
0.6–34.3
16.1
6.1
10.0
2.3
10
4
10
4
10
4
10
4.0
10.0
4.0
10.0
4.0
10.0
4.0
10.0
4.0
10.0
4.0
10.0
4.0
10.0
4.0
10.0
4.0
10.0
1
10
N25
30
35
25
25
25
35–36
35
25
19
Kulkarni and Joshi, 1980
Liao and Murai, 1986
Suárez and Xiques, 1969
Suárez and Xiques, 1969
Martı́nez and de la Cruz, 1985
Villareal and Ocampo, 1993
35
35
35
35
35
35
40
40
40
40
40
40
30
30
30
30
30
30
20
20
20
20
20
20
25
25
30
30
25
25
20
20
20
20
30
30
35
35
20
20
30
30
35
35
20
20
30
30
35
35
25
25
315.80
2870
375.28
344.14
383.70
295.26
181.43
716.29
478.63
412.48
316.23
409.86
223.87
256.62
193.37
449.04
387.70
720.51
537.77
170.66
137.40
251.80
226.04
407.10
313.83
201.63
140.76
335.07
286.61
512.50
366.85
366.29
284.19
L. vannamei a
L. vannamei a
L. vannamei a
L. stylirostris a
L. stylirostris a
L. stylirostris a
L. stylirostris a
L. stylirostris a
L. stylirostris a
L. stylirostris a
L. stylirostris a
L. stylirostris a
X. kroyeri
a
Juvenile shrimp.
Martı́nez-Palacios et al., 1996
Martı́nez-Palacios et al., 1996
Martı́nez-Palacios et al., 1996
This work
This work
This work
This work
This work
This work
This work
This work
This work
Carvalho and Phan, 1997
M. Spanopoulos-Hernández et al. / Aquaculture 244 (2005) 341–348
h1). In the present work, the QO2 at 40 at 20 8C and
30 8C was less than that found for L. vannamei
(Martı́nez-Palacios et al., 1996) and less than those
reported for P. japonicus (Kulkarni and Joshi, 1980)
(Table 6).
QO2 in juvenile L. stylirostris was inversely
proportional to body weight, with a mean slope of
0.74. This was lower than the values reported by
Scelzo and Zúñiga (1987) for F. brasiliensis and by
Carvalho and Phan (1997) for Xiphopenaeus kroyeri,
the mean values being 0.79 and 0.84, respectively. In
general, at a given temperature, salinity had no
significant effect on QO2 although the lowest QO2
was consistently recorded at 30, with higher values at
20 and 40. The increased metabolic rate at lower and
higher salinities suggests that L. stylirostris are in
group 2 of the Kinne classification (Kinne, 1967). At
30, juveniles of L stylirostris are close to the isoosmotic point, as was reported by Chim et al. (2003).
In considering the combined effect of salinity and
temperature on the respiratory rate of juvenile L.
stylirostris, several authors have shown that temperature is the factor having the greatest effect on
metabolic rate (Bishop et al., 1980; Kulkarni and
Joshi, 1980; Martı́nez-Palacios and Ross, 1986;
Martı́nez-Palacios et al., 1996). Clifford (1998)
suggested a maximum recommended temperature
between 30 to 31 8C with salinity in the range of 15
to 45, because L. stylirostris are sensitive to very low
salinities (0 to 5). Bassanesi (1982) showed that L.
stylirostris was sensitive to very low salinities and to
elevated temperatures but was less affected at lower
temperature (b35 8C) and hence the combined effect
of high salinity–high temperature results in elevated
oxygen consumption.
The polynomial model obtained in this work for
weight-specific oxygen consumption between salinities of 20 and 40 and temperatures of 20 to 35 8C in
shrimps over a weight interval from 4 to 14 g wet
body weight (Fig. 1) allows prediction of the
metabolic response of juvenile L. stylirostris and
shows the weight-specific oxygen consumption within
the range of culture operations normally encountered
in Mexico. The lowest QO2 in L. stylirostris is in the
temperature range 20 to 30 8C and between salinities
of 26 to 40. These parameters coincide with conditions found in the winter months of November to
March in Sinaloa and other areas on the Pacific coast
347
of Mexico and Central America where the species is
cultured.
Acknowledgements
The authors wish to acknowledge the financial
support of CONACyT, Mexico, through project
0556P-N9506 and the National Council of Technological Education for financial support through project
P-655.96. LGR wishes to acknowledge the support of
the British Council.
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